Basics of Functional Echocardiography in Children and Neonates
Basics of Functional Echocardiography in Children and Neonates
Basics of Functional Echocardiography in Children and Neonates
Basics of Functional
echocardiography in Children
and Neonates
Cécile Tissot1*, Vincent Muehlethaler 2 and Nicole Sekarski 3
1
Centre de Pediatrie, Clinique des Grangettes, Chêne-Bougeries, Switzerland, 2 Service de Pediatrie, Hôpital du Jura, Site de
Delémont, Delémont, Switzerland, 3 Pediatric Cardiology Unit, Department of Pediatrics, Centre Hospitalier Universitaire
Vaudois (CHUV), Lausanne, Switzerland
Functional echocardiography has become an invaluable tool in the pediatric and neo-
natal intensive care unit. “Point-of-care,” “target,” or “focus” echocardiography allows
bedside cardiac ultrasound evaluation of the hemodynamic status of the patient, helps
in directing treatment, thus improves patients care. In order to be able to perform func-
tional echocardiography, it is essential to understand the principles of ultrasound, to
know the echocardiographic equipment and settings necessary to acquire the images.
Edited by:
This article focuses therefore on the basics of cardiac ultrasound. It is meant to give an
Oswin Grollmuss, overview of two-dimensional echocardiographic views, M-mode imaging and Doppler
Université Paris-Sud, France
echocardiography for neonatologists and pediatric intensivists. It is richly illustrated for
Reviewed by:
better understanding with some examples of clinical applications of functional echocar-
Madhusudan Ganigara,
Mount Sinai Medical Center, diography in the intensive care setting.
United States
Giuseppe Limongelli, Keywords: echocardiography, target, point-of-care, intensive care, neonatology, pediatric, functional, bedside
cardiac ultrasound
Ospedale Monaldi, Università
degli Studi della Campania
‘L. Vanvitelli’, Italy INTRODUCTION
*Correspondence:
Cécile Tissot Functional echocardiography has become an invaluable tool in the pediatric and neonatal intensive
[email protected] care unit (1–6). Coupled with a clinical examination and monitoring techniques, echocardiogra-
phy can provide real-time rapid and reliable diagnostic answers that are invaluable to patient care.
Specialty section: This non-invasive bedside test has been developed over the past years to practice “point-of-care,”
This article was submitted to “target,” or “focus” echocardiography and can be used at the patient’s bedside to evaluate cardiac
Pediatric Cardiology, anatomy, to estimate intracardiac pressures and pressure gradients across valves and vessels, to
a section of the journal determine the direction of blood flow, pressure gradient across a defect, and to estimate filling
Frontiers in Pediatrics
pressure and fluid responsiveness. Functional echocardiography is useful to quantify ventricular
Received: 02 January 2017 systolic and diastolic function, to evaluate hemodynamics, to detect the presence of vegetation
Accepted: 17 October 2017
from endocarditis, to examine for the presence of pericardial fluid and for chamber or vessel
Published: 01 December 2017
thrombi. The characteristics of functional or “point-of-care” echocardiography are summarized in
Citation: Table 1. The primary barrier to future universal adoption of this operator dependent “stethoscope
Tissot C, Muehlethaler V and
of the future” is the lack of widespread, efficient, and affordable training solution. The need and
Sekarski N (2017) Basics of
Functional Echocardiography in
demand for training in functional echocardiography has grown in parallel to the expanded use
Children and Neonates. of ultrasound technology and to the development of portable machines. However, as with all
Front. Pediatr. 5:235. tools, a thorough understanding of its uses and limitations are necessary prior to relying on the
doi: 10.3389/fped.2017.00235 information it provides.
Table 1 | Characteristics of point-of-care echocardiography. Special care should be taken to adjust the ultrasound machine
Well-defined purpose linked to improving care of patients to optimize the echo image. Most echocardiography machines
Focused and goal-directed have a single button to adjust and optimize the image. There
Findings are easily recognizable and easily learned remain some simple adjustments that can help optimize image
Quickly performed acquisition. The choice of transducer is the most important for
Performed at the patient’s bedside
enhancing image quality. It is important to choose appropriate
presets, particularly for color Doppler. The image depth should
be adjusted so that the heart fills the viewing screen. The 2D
gain is used to adjust the strength of the returning echoes and
PRINCIPLES OF ECHOCARDIOGRAPHY
may be controlled in two ways. Overall gain may be changed to
Echocardiography utilizes ultrasound technology to obtain enhance the brightness of the image. Additionally, time-gain
images of the heart and vascular structures. Ultrasounds are compensation allows changes to the gain at various depth of
sound frequencies higher than the audible range of 20,000 interest and is controlled by a set of horizontal slide bars. The
cycles per second. The ultrasound machine consists of a central contrast can be improved by adjusting the compression or
processor and a transducer which can convert mechanical dynamic range. Echo machines also allow adjustment to the
energy (sound) from electrical energy and vice versa through beam focus.
piezoelectric crystals within the transducer. This will gener-
ate mechanical energy through a series of sinusoidal cycles of THE ANATOMICAL
alternating compression and rarefaction. This produced energy
passes as a beam to the heart. The beam travels in a direct line
ECHOCARDIOGRAPHIC EXAMINATION
until it finds structures with different acoustical impedance, OF A NORMAL HEART
such as between blood and tissue. When this happens, some
In order to remove respiratory artifacts, patients are placed in a
energy is reflected back to the same piezoelectric crystals and
left lateral decubitus position whenever possible. All planes refer
the remaining milder signal is transmitted distally. The reflected
to the axis of heart and not to its position within the body. The
energy also called ultrasound echoes will construct the cardiac
different views are obtained from standard windows. Segmental
image. Depending on the tissue characteristics, the portion of
approach is the preferred way of imaging the heart, especially for
acoustic energy transmitted versus reflected will vary. Anything
checking cardiac anatomy, and the situs and laterality need first
preventing the acoustic signal reflection, for instance air, bone,
to be determined, especially in the newborn. Thereafter, each
bandages, or other foreign bodies, will decrease the quality of the
cardiac structure is examined and described from the systemic
images. This is unfortunately a frequent problem in the intensive
and pulmonary venous return through the atria, ventricles, and
care unit (7).
great vessels.
Each cardiac structure is morphologically recognizable (8–10).
ECHOCARDIOGRAPHY EQUIPMENT AND The atrial septum has a right and left side with the foramen ovale
flap on the left side and the Eustachian valve on the right side.
SETTINGS The left and right atrium (RA) can be distinguished by looking
In order to perform functional echocardiography, it is necessary at their atrial appendages: the left atrial appendage is thin and
to have an ultrasound machine including a two-dimensional long, and the right atrial appendage is wide and triangular. The
(2D) mode, M-mode, pulsed-wave (PW), and continuous-wave atrioventricular valves always belong to the appropriate underly-
(CW) Doppler as well as color flow Doppler mapping. To be ing ventricle. The tricuspid valve is composed of three leaflets,
able to evaluate systole and diastole, electrocardiogram gating lies more toward the apex, has septal attachments and is associ-
is required. A storage system and the possibility to measure ated with the morphologic right ventricle. The mitral valve’s two
structures and velocities off-line are advantageous as it permits leaflets are attached to the lateral wall of the left ventricle by two
comparison between the studies. papillary muscles with no septal attachment and are associated
The motion of the heart requires the use of greater frame rate, with the morphologic left ventricle. The right ventricle is heavily
which is enhanced by beam focusing. Because of very different trabeculated and has the moderator band while the left ventricle
patient sizes in pediatrics, ranging from the newborn to the is smoothly walled. The aorta gives rise to the head and neck ves-
adult patient, several transducers with different frequencies are sels and the coronary arteries. The pulmonary artery gives rise to
necessary, ideally from 12 to 2.5 MHz. This allows for imaging the right and left branch pulmonary arteries.
at different depths. Higher frequency transducers have higher
resolution but less depth of penetration than lower-frequency STANDARD WINDOWS AND VIEWS
transducers. High frequency probes focus at depth of 4–5 cm
compared to low frequency probes able to focus at 12–16 cm. The standard windows for echocardiography in children include
For this reason, high frequency probes are used in neonates and the parasternal views (high left thorax just lateral to the sternum),
small children whereas low frequency probes are used in adults the apical views (left lateral thorax just inferior and lateral to the
with mid-range frequency transducer used in toddlers or small nipple), the subcostal views (below the xiphoid region), and the
children. suprasternal view (in the suprasternal notch) (Figures 1A–F).
Figure 1 | Continued
Figure 1 | Continued
Parasternal Window the left ventricle has a circular shape with symmetric contraction.
The parasternal view looks at the heart aligned along its long and The right ventricle is trabeculated and crescent-wrapping around
short axis. In the long axis view (Figure 1A), the left ventricular the left ventricle. Sweeping further to the base of the heart will
inflow and outflow tracts can be imaged. The aorta, including show the mitral valve and the papillary muscles. Continuing to
the annulus, the sinuses of Valsalva, and the proximal portion the base of the heart will allow imaging of the tri-leaflet aortic
of the ascending aorta can be observed, as well as its relationship valve in the center of the image with the right ventricular outflow
to the mitral valve (mitro-aortic continuity). The left ventricular tract and pulmonary artery wrapping anteriorly and to the left.
infero-posterior wall and interventricular septum are visualized. Part of the atrial septum and the tricuspid valve may be seen on
The anterior and posterior leaflets of the mitral valve can be the right side. Progressive sweep permits the examination of the
examined. By angulating the transducer posteriorly, the right atrial appendages, ascending aorta in cross-section and branch
ventricular inflow tract with the tricuspid valve can be imaged. pulmonary arteries.
If the transducer is angulated anteriorly, the right ventricular
outflow tract is visualized, including the pulmonary valve. Ninety Apical Window
degrees clockwise rotation will provide a short axis view of The apical view (Figure 1C) allow for visualization of all four
the heart (Figure 1B). Short axis views allows for evaluation of the chambers with the heart valves in a left-to-right orientation. The
heart chambers, the semilunar and atrioventricular valves, and the four-chamber view identifies the anatomic right and left ventricles.
coronary arteries. The ventricular chambers can be examined by Sweeping posteriorly will allow visualization of the coronary sinus
sweeping from the apex toward the base of the heart. In this view, in the left atrioventricular groove. Sweeping anteriorly will give the
Figure 1 | Continued
Figure 1 | Standard echocardiographic image planes from the high left chest just lateral to the sternum [parasternal window (A,B)], the left lateral chest just
inferior and lateral to the nipple [apical window (C)], sub-xyphoid area [subcostal window (D,E)], and the suprasternal notch [suprasternal window (F,G)]. Ao, aortic
valve; CS, coronary sinus; LA, left atrium; LV, left ventricle; PA, pulmonary artery; RA, right atrium; RV, right ventricle; RVOT, right ventricular outflow tract; SVC,
superior vena cava. Adapted from Ref. (1).
five-chamber view, where the atrial and ventricular septa may be the four-chamber view will produce a two-chamber view of the left
imaged and the left ventricular outflow tract and ascending aorta ventricle and left atrium. This view is the best to evaluate anterior
may be examined. The mitral valve leaflets can also be seen in this and posterior left ventricular wall function.
view, as well as the pulmonary veins as they enter the left atrium.
Turning the transducer 60° clockwise will bring a three-chamber Subcostal Window
view which shows the sub-aortic structures. This represents the The subcostal view (Figures 1D,E) provides the most comprehen-
best view to assess for Doppler measurement of the left ventricular sive information. Children are placed supine with the transducer
outflow tract. Turning the transducer 90° counterclockwise from in the subxiphoid position. In older cooperative children, better
image quality may be achieved by having the child hold his breath can be estimated by measuring the left ventricular volume in
allowing the heart to move downwards toward the transducer. end-diastole (LVEDV) and end-systole (LVESV) from an apical
Transverse views should determine visceral situs as well as the four-chamber view (Figure 2B). The ejection fraction (EF) is
relationship of the inferior vena cava and aorta. Sweeps will calculated using the following equation:
provide detailed imaging of the atrial and ventricular septum,
the atrioventricular valves, the atrial and ventricular chambers, LVEDV − LVESV
EF ( % ) = × 100.
and systemic venous return. Rotating the transducer will permit LVEDV
to image both right and left ventricular outflow tracts. Even the
peripheral pulmonary arteries and entire aorta may be examined Two-dimensional echocardiography is the method of choice
from this position in some patients. In some children with lung to diagnose pericardial effusion and to assess for cardiac
disease or in intensive care patients with poor acoustic windows, tamponade. Pericardial effusion appears as an echo-free space
this is the best view to obtain adequate imaging of the heart. between the two pericardial layers (Figure 3A), best seen from
the parasternal long axis view or from the subcostal views. The
size of the echo-free space depends on the amount of fluid and
Suprasternal Window
varies with the cardiac cycle. It should always be measured during
The suprasternal view is obtained by placing the transducer
diastole, to allow for reproducibility. Hemodynamic significance
in the suprasternal notch with the child’s neck extended and
of a pericardial effusion does not depend only on the amount of
slightly turned to the left. The suprasternal long and short axis
pericardial fluid and cardiac tamponade can be seen even with
(Figures 1F,G) views give information regarding the side of the
small effusion when the accumulation is rapid or with localized
aortic arch, the ascending and descending aorta with the head
effusion as seen after cardiac surgery. Echocardiographic signs
and neck vessels, the size and branching of the pulmonary arter-
of cardiac tamponade are late diastolic right atrial free wall col-
ies, as well as anomalies of the systemic and pulmonary venous
lapse, early diastolic right ventricular collapse, and significant
return. A patent ductus arteriosus can also be imaged in this view.
respiratory variation in tricuspid, mitral, and/or aortic (>25%)
Doppler flow pattern. Cardiac tamponade is also characterized
M-MODE ECHOCARDIOGRAPHY by increased right heart filling pressure. Echocardiography does
not produce accurate estimates of filling pressure but signs of
M-mode echocardiography is useful to evaluate cardiac dimen- increased right heart filling pressure are a dilated inferior vena
sions, timing with the cardiac cycle and function, and is best cava with loss of respiratory variation (Figure 3B).
obtained from the parasternal long or short axis view (11). The
M-mode image is produced by a single line of interrogation that
is repeatedly produced, with the picture displayed with the time DOPPLER ECHOCARDIOGRAPHY
along the x axis and with the distance from the transducer along
Movement of the blood or myocardium is provided by looking
the y axis (Figure 2A). M-mode is mainly used to estimate ven-
for Doppler shift in the reflected ultrasound waves. The Doppler
tricular function and wall thickness. Left ventricular function can
principle is based on the theory that for an immobile object, the
be estimated by measuring the left ventricular dimension in end-
frequency of ultrasound reflected is equal to the transmitted
diastole and end-systole (LVEDD and LVESD). The fractional
frequency. Moving objects change the frequency of the Doppler
shortening (FS) is calculated using the following equation:
shift according to the direction and velocity with which they are
LVEDD − LVESD moving in relation to the transducer (13).
FS ( % ) = × 100.
LVEDD
Spectral Doppler
This method relies on the assumption of a cylinder shape of Intracardiac and vascular hemodynamics may be obtained when
the ventricle (Simpson rule), and the estimation is altered in velocities are measured. Pulsed-wave (PW), continuous-wave
certain circumstances (single ventricle, right ventricle, globular (CW) modes, and color flow Doppler are essential for a complete
left ventricle). evaluation in children. Spectral Doppler velocities are recorded for
all the valves (mitral, tricuspid, aortic, and pulmonary), the main
2D ECHOCARDIOGRAPHY pulmonary artery and its branches, the ascending and descending
aorta, the pulmonary veins, and vena cava. Physiologic tricuspid
Two-dimensional echocardiography provides direct visual and pulmonary valve regurgitation is seen in 83 and 93% of
assessment of the beating heart, allowing for evaluation of the normal individuals (14).
size of the cardiac chambers, thickness of the walls, valve and Doppler data are typically displayed as velocity. The velocities
ventricular function, volume status, and presence of pericardial can then be transformed into pressure data using the modified
effusion. Bernoulli equation: P1 − P2 = 4 [(V2)2 − (V1)2]. Assuming that the
The systolic cardiac function depends upon left ventricular level of obstruction and therefore the velocity of V1 is trivial com-
contractility, preload, afterload, and heart rate. The cardiac pared with the obstruction at V2, the formula becomes simpler
function can be visually assessed and classified into normal or and is known as the modified Bernoulli equation: ΔP = 4(Vmax)2.
reduced to a mild, moderate, or severe degree. The left ventricular The modified Bernoulli equation helps estimate the pressure
ejection fraction is the best indice of left ventricular function and gradient and the severity of stenosis across a valve (Figure 4):
Figure 2 | M-mode echocardiography (A) obtained from the parasternal long axis view through the right and left ventricular chambers at the tip of the mitral valve
leaflets, allowing for the estimation of the fractional shortening. Two-dimensional echocardiography (B) obtained from an apical four-chamber view with tracing of the
endocardial LV border during end-diastole and end-systole, allowing for estimation of the ejection fraction. IVS, interventricular septum; LV, left ventricle; LVEDD, left
ventricular end-diastolic dimension; LVESD, left ventricular end-systolic dimension; LVPW, left ventricle posterior wall; RV, right ventricle. Adapted from Ref. (12).
Figure 4 | Spectral Doppler tracing (picture above) from aortic valve stenosis (AS) showing Vmax of 2.63 m/s, allowing for estimation of a pressure gradient across
the valve of 28 mmHg, consistent with moderate aortic valve stenosis. Spectral Doppler tracing (below picture) from tricuspid regurgitation (TR) showing Vmax of
3.94 m/s, allowing for estimation of a SPAP of 62 mmHg + RAP. RAP, right atrial pressure; SPAP, systolic pulmonary artery pressure.
rate is set so high that the signal from one pulse does not finish valve Doppler tracing show two phases: flow in early diastole,
its return before the next pulse is conveyed. Thus, Doppler shift representing early passive ventricular filling, is characterized
are detected from more than one interrogation site. by a peak wave called the E wave. It is followed by the A wave,
PW Doppler uses shot bursts of ultrasound signals trans- representing late ventricular filling during atrial contraction
mitted at regular intervals (PRF). PW is used to record the (Figure 7) (17). The mitral valve peak velocity is slightly
velocity across the valves, by placing the sample volume higher than that of the tricuspid valve (18). The flow in the
slightly proximal to the valve. The pulmonary and aortic valve pulmonary vein is continuous with a diastolic (D wave) and
Doppler tracing is a unique envelope with a peak velocity of a systolic (S wave) peak. The diastolic peak velocity is usually
approximately 1 m/s (Figure 7). The tricuspid and mitral higher than the systolic. Often, flow reversal (A wave) can
Figure 5 | Spectral Doppler (A) obtained through a VSD with high velocity
left-to-right shunt and no pulmonary hypertension (above picture) and with low
velocity left-to-right shunt and pulmonary hypertension (below picture). The
pressure gradient across the VSD allows for estimation of the systolic PAP.
Spectral Doppler (B) obtained through a PDA with high velocity left-to-right
shunt and no pulmonary hypertension (above picture) and with low velocity
left-to-right shunt and pulmonary hypertension (below picture). The pressure
gradient across the PDA allows for estimation of the systolic PAP. BP, systolic Figure 7 | Comparison of pressure curve of the aorta (Ao), left ventricle (LV),
blood pressure; LV, left ventricle; PAP, pulmonary artery pressure; PDA, patent left atrium (LA) and velocity across the left ventricular outflow tract (LVOT) and
ductus arteriosus; RV, right ventricle; VSD, ventricular septal defect. left ventricular inflow (LV inflow) and spectral Doppler from pulse wave across
the LVOT (aortic valve) from apical five-chamber view and LV inflow (mitral valve)
from apical four-chamber view. E, early diastolic ventricular filling wave; A, late
diastolic ventricular filling during atrial contraction wave. Adapted from Ref. (12).
be seen during atrial contraction. This flow pattern does not
vary with respiration (19). Vena cava flow is a continuous low
velocity flow but the peak velocity is greater in systole (S wave) to adults. Respiratory variation is seen with augmentation of
compared to diastole (D wave). Flow reversal during atrial flow velocities during inspiration (17). Hepatic venous flow
contraction (A wave) occurs less often in children compared shows a predominantly systolic biphasic flow pattern (20).
Tissue Doppler
Doppler can be applied to measure myocardial rather than
blood velocities. The difference resides in filtering: imaging
myocardial velocities requires filtering structures that are mov-
ing at high velocity with low scattering power (i.e., the blood)
while imaging blood velocity requires filtering out slowly mov-
ing and strongly reflecting structures (i.e., the myocardium).
Tissue Doppler imaging is helpful for assessing systolic and
diastolic myocardial function (21–24). In a four-chamber
view, the cursor should be placed at the junction between the
ventricles and atria over the interventricular septum, on the
Figure 8 | Color Doppler flow mapping with Blue directed away from the lateral wall of the left ventricle and on the lateral wall of the
probe and red directed toward the probe: mnemotechnic = BART.
right ventricle. The tracing includes early diastolic (E′), late
diastolic (A′), and systolic (S′) waves (Figure 9). Age based
normal values in children are available (25–27).
Hospital of Geneva (HUG) until recently and is now working in du Jura, Delemont, Switzerland. The three authors are part of
the Pediatric Center at Clinique des Grangettes, Switzerland. NS the organizing committee of the Training in Intensive Care and
is a pediatric cardiologist trained at the University Hospital of Neonatal Echocardiography (TINEC), a course on point-of-care
Lausanne and in Washington University, Saint-Louis, USA. NS is echocardiography that is taking place in Lausanne, Switzerland,
working as the chief of the Pediatric Cardiology Unit at the Centre since January 2016.
Hospitalier Universitaire Vaudois (CHUV). VM is a neonatolo-
gist trained at the University Hospital of Lausanne, Switzerland, AUTHOR CONTRIBUTIONS
in Denver, Colorado, USA, and in Sydney, Australia. VM has
been working as an attending neonatologist at the CHUV until All authors listed have made a substantial, direct and intellec-
recently and is now working in the Pediatric Service at Hopital tual contribution to the work, and approved it for publication.
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