Longitudinal systolic left ventricular function in preterm and term neonates: reference values of the mitral annular plane systolic excursion (MAPSE) and calculation of z-scores

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Pediatric Cardiology ISSN 0172-0643 Pediatr CardiolDOI 10.1007/s00246-014-0959-6

Longitudinal Systolic Left VentricularFunction in Preterm and Term Neonates:Reference Values of the Mitral AnnularPlane Systolic Excursion (MAPSE) andCalculation of z-ScoresMartin Koestenberger, Bert Nagel,William Ravekes, Andreas Gamillscheg,Corinna Binder, Alexander Avian,Jasmin Pansy, et al.

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ORIGINAL ARTICLE

Longitudinal Systolic Left Ventricular Function in Pretermand Term Neonates: Reference Values of the Mitral AnnularPlane Systolic Excursion (MAPSE) and Calculation of z-Scores

Martin Koestenberger • Bert Nagel • William Ravekes • Andreas Gamillscheg •

Corinna Binder • Alexander Avian • Jasmin Pansy • Gerhard Cvirn •

Berndt Urlesberger

Received: 13 January 2014 / Accepted: 20 June 2014

� Springer Science+Business Media New York 2014

Abstract The mitral annular plane systolic excursion

(MAPSE) is a quick and reliable echocardiographic tool for

assessing longitudinal left ventricular (LV) systolic func-

tion in children and adults. Because this parameter is

affected by the LV longitudinal dimension, pediatric and

adult normal values are not suitable for preterm and term

neonates. A prospective study investigated a large group of

preterm and term neonates [gestational age (GA), 26/0–6 to

40/0–6; birth weight (BW), 670–4,140 g]. The growth- and

BW-related changes in MAPSE were determined to

establish normal z-score values for preterm and term neo-

nates. The MAPSE ranged from a mean of 0.36 ± 0.05 cm

in preterm neonates with a GA of 26/0–6 to

0.56 ± 0.08 cm in term neonates with a GA of 40/0–6. The

findings showed MAPSE, GA, and BW to be moderately

correlated. Pearson’s correlation coefficient was 0.56 for

GA (MAPSE; p \ 0.001) and 0.58 for BW (MAPSE;

p \ 0.001). The normal MAPSE values did not differ

significantly between females and males (p = 0.946). The

absolute values and z-scores of normal MAPSE values in

healthy preterm and term neonates within the first 48 h of

life were calculated, and percentile charts were established.

Determination of LV function using MAPSE might be

useful for vulnerable infants for whom a prolonged

examination is inappropriate and for neonates with sub-

optimal visualization of the endocardium.

Keywords Mitral annular plane systolic excursion � Left

ventricular long-axis function � Preterm � Neonates �Reference values � Birth weight � M-mode � z-Score

Introduction

The mitral annular plane systolic excursion (MAPSE) is

reported to correlate well with left ventricular ejection

fraction (LVEF) in adults [7, 28]. Findings have shown

MAPSE, an M-mode—derived measure of longitudinal LV

function [21], to be an important parameter of the global

LV function in premature infants as well [8, 33].

The morphology of the preterm heart shows a thinner

walled left ventricle (LV) and a functionally hypertrophied

right ventricle (RV) [32]. After birth, ductal shunting rapidly

changes from balanced to left-to-right shunting, with a

responsive increase in LV stroke volume [26, 27]. Especially

in cases of noncooperative and vulnerable infants for whom

prolonged examination may be inappropriate or in cases

involving an endocardium that is suboptimal for tracing,

determination of the MAPSE may be a useful technique.

However, the MAPSE is growth dependent.

M. Koestenberger (&) � B. Nagel � A. Gamillscheg

Division of Pediatric Cardiology, Department of Pediatrics,

Medical University Graz, Auenbruggerplatz 34/2, 8036 Graz,

Austria

e-mail: [email protected];

[email protected]

W. Ravekes

Division of Pediatric Cardiology, Johns Hopkins University

School of Medicine, Baltimore, MD, USA

C. Binder � J. Pansy � B. Urlesberger

Division of Neonatology, Department of Pediatrics, Medical

University Graz, Graz, Austria

A. Avian

Institute for Medical Informatics, Statistics and Documentation,

Medical University Graz, Graz, Austria

G. Cvirn

Institute of Physiological Chemistry, Center of Physiological

Medicine, Medical University Graz, Graz, Austria

123

Pediatr Cardiol

DOI 10.1007/s00246-014-0959-6

Author's personal copy

Normal MAPSE values in healthy children have been

published recently [17]. Eriksen et al. [9] have shown that the

annulus excursion of both atrioventricular (AV) valves var-

ies with ventricular size and that the MAPSE as well as tissue

Doppler imaging (TDI) parameters may be useful and easily

available methods for the evaluation of LV function.

Changes in systolic LV function determined by MAPSE

in the early neonatal period may give sufficient information

about LV function in preterm and term neonates. The

MAPSE is not a measure of the percentage of LV long-axis

shortening, so smaller persons with a smaller LV may have

a smaller MAPSE. For full assessment of changes in the

systolic LV function of patients with congenital heart

defects (CHD), healthy neonates, and neonates with sepsis

or asphyxia and need for cooling, requires sufficient

quantitative reference data. Therefore, reference values for

neonates and determination of the effect of gestational

week and birth weight (BW) are crucial.

We therefore undertook a prospective study to deter-

mine normal values for MAPSE within the first 48 h of life

in correlation with week of gestation and BW and to cal-

culate normal z-score values in a cohort of 261 preterm and

term neonates (ages, 26/0–6 to 40/0–6 weeks of gestation).

Materials and Methods

Patient Population

The patients were selected from individuals referred to the

neonatal intensive care unit for observation or to our car-

diology service for evaluation of a heart murmur or a

family history of heart disease during the first 2 days of

life. The gestational age (GA) was determined from the last

menstrual period and confirmed by accurate estimation

obtained by the patients’ obstetricians. The criteria for

inclusion in the study specified that the measured LVEF

(Simpson’s method) had to be higher than 60 %, the LV

fractional shortening (M-mode) had to be higher than 30 %

in all patients, and a measured tricuspid annular plane

systolic excursion had to be within the published age-

related normal z-score values [16]. Patients who were small

for GA (SGA) at birth were excluded from the study. All

infants with suspected malformations and those with sus-

pected or proven sepsis or septic shock, asphyxia, or need

for inotropic and chronotropic drugs also were excluded.

The infants were classified as having proven early-onset

sepsis (positive blood culture), clinical early-onset sepsis

(negative blood culture but clinical signs of sepsis with a

positive sepsis screen or a history of risk factors and

antibiotic treatment C7 days), or a negative infectious

status (negative blood culture, negative sepsis screen,

antibiotic treatment B3 days) [29]. Septic shock was

defined as sepsis in the presence of cardiovascular dys-

function. Arterial hypotension was defined as an oscillo-

metric mean arterial blood pressure below 95 % limits,

requiring treatment. Patients with suspected pulmonary

hypertension were excluded from this study.

Perinatal data including Apgar scores at 1 and 5 min, pH

of the umbilical artery, and mode of delivery were recor-

ded. For the purpose of the study only echocardiograms

with an official reading of a completely normal study were

accepted for analysis except for patent foramen ovale

(PFO) with a diameter of 2 mm or less. None of our

patients had a diagnosis of a hemodynamically significant

persistent ductus arteriosus (PDA). A PDA was diagnosed

as hemodynamically important if it fulfilled the following

three echocardiographic criteria: a left atrium-to-aortic root

diameter ratio of 1.4 or greater, an internal ductal diameter

greater than 1.4 mm/kg, and a left pulmonary artery end-

diastolic flow greater than 0.2 m/s.

The PDA constricts quickly after birth, but findings have

shown some shunting to be commonly apparent on color

Doppler mapping during the first 12–24 h of life [10]. In all

our preterm infants younger than 29 gestational weeks, a

standard prophylactic indomethacin administration was

started on day 1. Some of the patients were included in

previous studies [16, 18].

We included only infants with a healthy respiratory con-

dition. All infants older than 28 gestational weeks who had any

need of supplemental oxygen were excluded from the study.

For infants younger than 28 gestational weeks, the definition

of a ‘‘healthy respiratory condition’’ may become difficult. For

this group of infants, noninvasive respiratory support with

nasal continuous positive airway pressure (CPAP) often is

necessary for maintenance of adequate functional residual

capacity [5]. We included only premature infants with the

need for nasal CPAP or supplemental oxygen who had a

fraction of inspired oxygen (FiO2) lower than 0.3. All infants

with supplemental oxygen whose FiO2 exceeded 0.3 and those

who had a need for intubation and mechanical ventilation

were excluded from the study. Furthermore, all infants with

any suspected anomalies of airways also were excluded.

Echocardiographic Techniques

Echocardiographic examination was performed within 48 h

after birth by two experienced echocardiographers (M.K.;

B.N.). Echocardiograms were performed with echocardio-

graphic systems (iE33; Philips, Andover, MA, USA) using

a transducer of 12–4 MHz. The images were recorded

digitally and later analyzed by one of the investigators

(M.K.) using offline software (Xcelera Echo; Philips

Medical Systems, Eindhoven, The Netherlands).

For determination of the LVEF, we used the modified

Simpson’s method, which is the most commonly used and

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recommended method [19]. The MAPSE was measured

using the standard M-mode technique, with the cursor

placed at the lateral site of the annulus from the apical four-

chamber view [35]. The long-axis excursion of the lateral

mitral ring was measured by determining the distance

between the nadirs of the annulus motion profile corre-

sponding to the maximal backward excursion of the mitral

ring from the apex, defined as the point of maximal upward

excursion. Care was taken to align the sample volume as

vertically as possible with respect to the cardiac apex.

To determine interobserver variability, data were mea-

sured by two observers (M.K.; B.N.) blinded to the results

of each other. Intraobserver variability was considered

among 24 participants by repeating measurements on two

occasions. Inter- and intraobserver variabilities were

examined with an intraclass correlation coefficient (ICC).

Statistical Analysis

All data (from 3 to 5 consecutive beats) were measured by two

well-trained observers (M.K.; B.N.) and averaged. Data are

presented as means ± standard deviations (SD). Regression

was used to estimate MAPSE from GA, BW, and sex.

In a first step, the correlation structure between continu-

ous variables and MAPSE was examined with the Pearson

correlation coefficient. Furthermore, group differences in

MAPSE between male and female neonates were examined

using the t test. Eligible variables with a significant corre-

lation or significant group differences were chosen for fur-

ther evaluation. Therefore, models using linear relations

were tested. The White test and the Breusch-Pagan test were

used to test for heteroscedasticity. When significant hetero-

scedasticity was detected, weighted least-square methods

were used. To test for normal distribution of z-scores, the

Anderson–Darling test and the Kolmogorov–Smirnov test

were used. For data analysis, SPSS 20 (SPSS, Inc., Chicago,

IL, USA) and SAS 9.2 (REG and MODEL procedure; SAS

Institute, Cary, NC, USA) were used. A p value lower than

0.05 was considered statistically significant.

Ethics

This study complied with all institutional guidelines related

to patient confidentiality and research ethics including

institutional review board approval. Prospective written

parental consent was obtained. There are no financial or

other potentially conflicting relationships to report.

Results

The study group consisted of 327 patients (171 males and

156 females), with a GA range of 26 ? 0 to 40 ? 6 weeks.

After the exclusion of neonates who did not meet the

inclusion criteria, 261 newborns (132 males and 129

females) with GAs ranging from 26/0–6 to 40/0–6 weeks

and BWs ranging from 670 to 4,140 g were available for

statistical analysis.

The MAPSE ranged from a mean of 0.36 ± 0.05 cm in

preterm neonates with a GA of 26/0–6 weeks to

0.56 ± 0.08 cm in neonates with a GA of 40/0–6 weeks. The

inter- and intraobserver variabilities were found to be good for

MAPSE, with ICCs of 0.96 [95 % confidence interval (CI),

0.94–0.98; p\0.01] and 0.97 (95 % CI, 0.95–0.99; p [0.01).

The characteristics of the study group are presented in

Table 1. The age-related z-scores ± 2 and ± 3 standard

deviations for MAPSE are shown in Table 2. A representative

M-mode image of the MAPSE (neonate with a GA of

29/3 weeks) with normal RV and LV function is shown in

Fig. 1.

The MAPSE values, measured within 48 h of life,

increased in a linear way from a GA of 26/0–6 to a GA of

40/0–6. Birth weight, MAPSE, and GA were moderately

correlated: Pearson’s correlation coefficient was 0.56 for

GA–MAPSE (p \ 0.001), 0.58 for GA–BW (p \ 0.001),

and 0.89 for BW–MAPSE (p \ 0.001). The female and male

neonates had comparable MAPSE values (p = 0.946).

Because of the strong correlation between GA and BW,

two separate models were calculated. The regression

equation relating GA (weeks) and MAPSE (cm) for cal-

culation of the predicted MAPSE (MAPSEpred) for a given

GA is MAPSEpred = 0.039 ? 0.013 9 GA. The GA-rela-

ted z-scores for MAPSE are shown in Table 2. The

Table 1 Characteristics of the study group

Gestational age (weeks) Median (Range) 34 (26–40)

Birth weight (kg) Median (Range) 2.33 (0.67–2.14)

Males (% of all) n 133 (51)

Caesarean section n 104

Apgars at 1 min Mean ± 2 SD 8.7 ± 0.45

Apgars at 5 min Mean ± 2 SD 9.3 ± 0.27

pH umbilical artery Mean 7.28

PDA n 93

PFO n 135

N-CPAP n 46

PEEP(NCPAP) Range 3.0–5.0

The range of GA and of BW, the sex of preterm and term neonates,

Apgar scores of 1 and 5 min (mean ± standard deviation), number of

patients with residual shunting on a PDA smaller than 1.5 mm in size,

number of patients with a PFO smaller than 2 mm in size, number of

patients delivered by cesarean section, number of patients with nasal

CPAP support, the PEEP under CPAP therapy, and the pH of the

umbilical artery are given

BW birth weight, CPAP continuous positive airway pressure, GA

gestational age, PFO patent foramen ovale, PDA persistent ductus

arteriosus, PEEP positive end-expiratory pressure, wks weeks, kg

kilogram, n number of patients, SD standard deviation

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regression equation relating BW (kg) and MAPSE (cm) is

MAPSEpred = 0.331 ? 0.060 9 BW. The BW-related z-

scores ± 2z and ±3z for MAPSE are shown in Table 2.

To investigate a possible effect of nasal CPAP therapy

on MAPSE values, we determined the MAPSE in 10

preterm neonates (GA, 26/0–6 to 28/0–6) without the need

for nasal CPAP support and in 10 GA-matched preterm

neonates receiving nasal CPAP therapy. The MAPSE val-

ues did not differ significantly between the two groups.

The data for all the neonates were analyzed to draw GA-

related ± two and three z-score values and BW-rela-

ted ± two and three z-score values. Graphs demonstrating

the mean value plus or minus two and three z-scores for

Table 2 Classification table for the MAPSE values

GA (week) n Observed

-3z -2z Mean ?2z ?32

26 11 0.21 0.26 0.36 0.46 0.51

27 10 0.24 0.28 0.38 0.48 0.53

23 12 0.17 0.25 0.4 0.55 0.62

29 13 0.23 0.29 0.42 0.54 0.6

30 14 0.18 0.26 0.42 0.58 0.66

31 15 0.26 0.32 0.45 0.58 0.65

32 15 0.19 0.27 0.43 0.59 0.67

33 22 0.14 0.24 0.44 0.64 0.74

34 23 0.3 0.36 0.48 0.6 0.66

35 10 0.26 0.34 0.49 0.64 0.72

36 17 0.25 0.33 0.48 0.63 0.71

37 13 0.22 0.31 0.5 0.68 0.77

38 32 0.35 0.41 0.53 0.65 0.71

39 39 0.22 0.32 0.52 0.71 0.81

40 15 0.31 0.4 0.56 0.73 0.81

BW (kg) n Observed

-3z -2z Mean ?2z ?32

0.8 10 0.2 0.26 0.37 0.48 0.54

1 13 0.21 0.26 0.35 0.45 0.5

1.2 25 0.23 0.29 0.4 0.51 0.57

1.4 15 0.29 0.35 0.47 0.58 0.64

1.6 20 0.13 0.23 0.42 0.62 0.72

1.8 13 0.21 0.29 0.44 0.59 0.67

2 15 0.23 0.3 0.44 0.59 0.66

2.2 17 0.27 0.33 0.47 0.6 0.67

2.4 22 0.25 0.33 0.5 0.66 0.74

2.6 14 0.31 0.38 0.51 0.63 0.7

2.8 15 0.25 0.33 0.49 0.65 0.73

3 17 0.21 0.3 0.48 0.65 0.74

3.2 24 0.26 0.35 0.53 0.71 0.8

3.4 15 0.31 0.38 0.52 0.66 0.74

3.6 13 0.33 0.4 0.53 0.67 0.74

3.8 7 0.4 0.46 0.58 0.7 0.77

4 6 0.25 0.36 0.57 0.78 0.89

The values in the classification table are shown as follows. (A) For

each GA, the observed and predicted means and ±2z and ±3z are

presented. (B) For the BW, the observed and predicted means and

±2z and ±3z are presented

BW birth weight, GA gestational age, MAPSE mitral annular plane

systolic excursion

Fig. 1 Apical four-chamber view. a The white broken line indicates

the M-mode cursor placement at the free wall of the mitral annulus as

recommended. b Representative M-mode image of the mitral annular

plane systolic excursion (MAPSE) in a preterm infant (born in the

29/3 week of gestation) with normal right and left ventricular

function. The absolute longitudinal displacement measure in centi-

meters (cm) is shown as the yellow line. The red line marks the upper

measure point as the point of maximal upward excursion

Fig. 2 Gestational week versus observed mean value of mitral

annular plane systolic excursion (MAPSE) ± 2 standard deviations

(SDs) for gestational week versus MAPSE. The mean is indicated by

the black solid line, the z-score ±2 by the black broken lines, and the

z-score ± 3 by the black dotted lines

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MAPSE versus GA and MAPSE versus BW are presented

in Figs. 2 and 3, respectively.

Discussion

To date, as part of the assessment of cardiac function in

neonates, increasing attention has been paid to the longi-

tudinal aspect of the LV function in the evaluation of LV

systolic function. The apical displacement with shortening

of the LV along its long axis can be measured by two-

dimensional echocardiography and M-mode. Conventional

methods for assessing systolic LV function such as EF and

fraction shortening (FS) are essentially independent of the

weight despite a marked increase in the size of the LV

during normal growth [13]. The LVEF is dependent on

cavity size and shown to be biased by strict load depen-

dency and low sensitivity to early impairment in fiber

contractility [11]. The MAPSE is considered to be a reli-

able index of longitudinal function in children and adults,

but it must be taken into account that the amount of dis-

placement is affected by LV longitudinal dimension.

Using tissue Doppler-derived strain and strain rate

measurements during the first 28 days of life in preterm

infants, Helfer et al. [12] showed that peak systolic strain

measurements determined in preterm infants with a patent

ductus arteriosus or a bronchopulmonary dysplasia reflect

both an increased afterload and an increased preload. In-

traobserver reproducibility deformation indices in neonates

were shown to be adequate for myocardial velocity imag-

ing parameters, whereas interobserver reproducibility were

shown to be suboptimal, suggesting that these measure-

ments should be used with caution in clinical practice [15].

Studies have shown that LV function parameters correlate

with age in neonates and children [3, 4, 9, 25, 30].

In a recent study, Lee et al. [20] demonstrated that

myocardial tissue velocities decrease significantly 5–12 h

after birth in preterm infants. In a study comparing cardiac

function measured by TDI, Ciccone et al. [4] demonstrated

that myocardial velocities are higher in preterm than in

term neonates. During the transition period from fetal to

neonatal life, changes in LV myocardial performance were

observed using TDI and speckle-tracking echocardiogra-

phy [14, 31]. In preterm neonates, significant changes in

myocardial function were observed immediately after PDA

ligation, suggesting important changes in myocardial per-

formance [6]. In neonates with asphyxia, findings have

shown the LV systolic function to be decreased [34]. Also,

neonates with congenital diaphragmatic hernia demon-

strated impaired LV function, a finding shown to be asso-

ciated with adverse outcomes in this group [1]. In addition,

changes in TDI parameters during the first year of life were

recently observed [2]. Therefore, it is crucial to have nor-

mal values for preterm and term neonates because normal

pediatric and adult values do not apply for these patients.

We found that MAPSE values increase with GA and

BW. Due to developmental changes, it is accurate not to

use a single value throughout the population but rather to

reference the MAPSE to both GA and to BW for the best

interpretation of the results. In this study, the MAPSE

values were lower in preterm than in term neonates.

Whether the markedly lower MAPSE in earlier weeks of

gestation is solely a marker of growth-related changes

within the study population or a sign of altered systolic

function in younger GA neonates due to the immaturity of

the LV musculature remains unclear. As expected, our

normal values for MAPSE in the 40/0–6 term neonates

were similar to the MAPSE normal reference values of

infants available in the literature [17].

In the current study, no significant differences in

MAPSE values were found between the male and female

neonates. We did not find significant differences in the

MAPSE values between 10 preterm neonates (GA, 26/0–6

to 28/0–6) without the need for nasal CPAP support and 12

GA-matched preterm neonates with CPAP therapy. This is

in agreement with data from different groups demonstrat-

ing that CPAP therapy has only a small effect on M-mode

measurements and does not change the cardiac output in

preterm infants [24].

In conclusion, we have established normal reference

values of MAPSE in preterm and term neonates within the

first 48 h of life in terms of GA and BW that could serve as

a reference database for preterm and term neonates with

CHD and suspected LV dysfunction. The M-mode—

Fig. 3 Birth weight versus observed mean value of mitral annular

plane systolic excursion (MAPSE) ± 2 standard deviations (SD) for

birth weight versus MAPSE. The mean is indicated by the black solid

line, the z-score ± 2 by the black broken lines, and the z-score ± 3

by the black dotted lines

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derived MAPSE is a noninvasive method for evaluation of

LV function that is an especially useful parameter in cases

of noncooperative and vulnerable infants for whom a

prolonged examination may be inappropriate or in cases

involving an endocardium that is suboptimal for tracing. In

the future, after more detailed validation, the MAPSE may

be included in the targeted neonatal echocardiography

guidelines [22] that allow neonatologists to assess the

ventricular function in newborns.

Study Limitation

A limitation of this study was that the MAPSE was mea-

sured only on the lateral site of the mitral annulus. We

focused on the lateral wall in the four-chamber view

because findings have shown this view to be reliable and

easy to apply even in younger children [17]. A possible

problem is that systolic translational motion of the heart

may influence the values measured [23]. Although MAPSE

is a good parameter for assessment of longitudinal LV

systolic function, it does not take into account segmental

LV function. We did not assess the effects of preload

variations related to respiration. In neonatal clinical prac-

tice, it would be cumbersome to apply respiratory gaiting

to this method on a routine basis.

This study was conducted with a cross-sectional study

design. Therefore, the data provided in this study should be

used only for neonates within the first 48 h of life. This

study was limited by the impossibility of defining ‘‘nor-

mal’’ respiratory support in premature neonates younger

than 28 gestational weeks. For this study, we recruited only

a relatively small number of preterm and term neonates for

each gestational week and recognize that this reduced the

power of our study to detect small changes in the MAPSE,

increasing the likelihood of a type 2 error. We must state

that it remains unclear how well MAPSE will perform as

an index of systolic LV function in neonates with con-

genital heart disease (CHD) compared with other potential

approaches (e.g., the myocardial performance index) or

newer LV deformation parameters (e.g., the ventricular

rotation) unless clinical studies prove its usefulness.

Conflict of interest All authors state that there are no financial,

personal or other relationships with other people or organizations that

could inappropriately influence our work to disclose.

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