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Ecocardiografia Neonatal
Ecocardiografia Neonatal
CURRENT
OPINION Neonatal functional echocardiography
Cecile Tissot a and Yogen Singh b,c
Purpose of review
The role of echocardiography has dramatically changed over the past decade and use of functional
echocardiography has become increasingly popular among neonatologists and pediatric intensivists in
making clinical decisions in sick infants and children. The purpose of this review is to outline the current
capabilities and limitations of functional echocardiography, best practices for its clinical application, and
evidence for its utility.
Recent findings
Functional echocardiography can provide direct assessment of hemodynamics at bedside and can be used
as a modern hemodynamic monitoring tool in the neonatal intensive care unit. It is now being regarded as
a useful extension to the clinical examination and other monitoring tools in the critically ill infant. The
anatomic, physiological, and hemodynamic information functional echocardiography provides can be used
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point-of-care cardiac ultrasound and clinician per- 1. Assessment of hemodynamics and cardiac func-
formed ultrasound to name a few. All the expert tion in neonatal hypotension and shock.
consensus statements have emphasized developing 2. Suspected patent ductus arteriosus (PDA).
a structured training program and accreditation pro- 3. Perinatal asphyxia or hypoxic-ischemic enceph-
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cess specifically designed for neonatologists [7,8 ,9 ]. alopathy.
Functional echocardiography performed in the 4. Suspected pulmonary hypertension of the new-
newborn in the neonatal intensive care unit (NICU) born (PPHN) or acute pulmonary hypertension.
differs significantly from that performed in older 5. Congenital diaphragmatic hernia.
children in the pediatric intensive care unit or pedi- 6. Suspected pericardial or pleural effusion.
atric emergency department because newborns with 7. Central line assessment.
hemodynamic instability are at a higher risk of 8. Extracorporeal membrane oxygenation cannula-
having an underlying undiagnosed CHD, especially tion.
within first 2–4 weeks after birth, and critical or
significant CHD must be ruled out in sick neonates. Table 1 summarizes the recommendations and
For this reason, the European and North American echo parameters for the practice of NPE. Ultrasound
expert consensus statements have emphasized that machines used for performing NPE should include
the first echocardiography performed in a newborn two-dimensional, M-mode, and Doppler capabili-
should include a comprehensive cardiac anatomy ties. A range of multifrequency probes (6–12 MHz)
assessment to rule out major CHD. This requires should be available. A simultaneous electrocardio-
specific training and expertise and close collabora- gram tracing should be displayed. Ideally, the stud-
tion with pediatric cardiology services. The subse- ies should be stored on a database to be easily
quent scans can be functional and focused or reviewed by other people. A detailed description
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targeted to address specific questions [7,8 ,9 ,10]. of echocardiographic techniques is beyond the
&&
scope of this article [11 ].
INDICATIONS AND BASIC REQUIREMENTS
FOR FUNCTIONAL NEONATAL ECHOCARDIOGRAPHIC EVALUATION OF
ECHOCARDIOGRAPHY HEMODYNAMICS AND CARDIAC
The most important concept is that neonatal func- FUNCTION IN NEONATAL HYPOTENSION
tional echocardiography is not intended to replace a AND SHOCK
thorough examination by a pediatric cardiologist or Neonatal shock is common in critically ill infants in
by a clinician trained in structural echocardiogra- NICU and carries a high mortality. The American Col-
phy. If structural CHD is suspected, the first echo- lege of Critical Care Medicine guidelines have empha-
cardiography should always be comprehensive to sized early recognition and instituting goal-oriented,
assess cardiac anatomy and function by using the time-sensitive interventions. These guidelines have
FAC, fractional area change; LVEDD, left ventricle end-diastolic dimension; LVESD, left ventricle end-systolic dimension; PAP, pulmonary artery pressure; PDA,
patent ductus arteriosus; PFO, patent foramen ovale; RVSP, right ventricle systolic pressure; SVC, superior vena cava; TAPSE, tricuspid annular plane systolic
excursion.
suggested using bedside echocardiography in identify- cardiomyopathy) [19]. Increased wall thickness can
ing the underlying pathophysiology, evaluating hemo- occur in pressure loading conditions (valve stenosis).
dynamics, and managing response to treatment in The systolic function of the left ventricle can be
patients with neonatal shock [12]. quickly assessed qualitatively by visual inspection
Functional echocardiography can help in assess- but this method is prone to interobserver variability.
ing preload, cardiac function, and afterload which It can also be assessed quantitatively by measuring
may help in understanding the underlying patho- the shortening fraction on M-mode from the para-
physiology for hemodynamic instability or poor sternal short-axis or long-axis views (Fig. 1). Ejection
cardiac output. This physiological information, in fraction calculated by planimetry using the modi-
conjunction with other clinical parameters and fied Simpson’s method may give a more accurate
monitoring tools, can be used in choosing fluid assessment especially in infants with septal flatten-
resuscitation therapy or appropriate inotropic or ing or paradoxical interventricular septal motion
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vasopressor/vasodilator therapy [13]. Although (e.g., in pulmonary hypertension) [20 ]. When
some infants with septic shock may need fluid interpreting shortening fraction and ejection frac-
resuscitation therapy, aggressive fluid boluses can tion, the influence of preload and afterload should
be hazardous in infants with cardiogenic shock. be taken into account. This is especially true when
Similarly, acute pulmonary hypertension is com- comparing cardiac function before and after ductal
mon in neonatal shock and early recognition of closure and explains the usual decrease in shorten-
increased pulmonary afterload may help in early ing fraction and ejection fraction seen immediately
institution of pulmonary vasodilators [3,14–16]. after surgical duct ligation.
Quantification of cardiac chambers and cardiac The anatomy and geometrical shape of the right
structure dimensions implies reporting the measure- ventricle do not permit using similar parameters for
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ments as Z scores [17 ,18]. Increased left ventricular assessing right ventricle systolic function [18,21–23].
end-diastolic dimension can be seen in volume load- Hence, right ventricle systolic function is often
ing conditions (shunt lesions or valve regurgitation) assessed by visual inspection but this is also prone
or in left ventricular dysfunction (dilated to interobserver variability. Tricuspid annular plane
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FIGURE 1. Left ventricle shortening fraction (LVSF) obtained from parasternal long-axis or short-axis view with normal LVSF (left
picture) and decreased LVSF (right picture) in a patient with dilated cardiomyopathy. White arrow indicates systolic
contraction of the left ventricular posterior wall. LVEDD, left ventricle end-diastolic dimension; LVESD, left ventricle end-systolic
dimension.
systolic excursion (TAPSE) (Fig. 2) or tissue Doppler including Doppler mitral or tricuspid inflow and
imaging (TDI) S0 -wave velocity (Fig. 3) are good pulmonary venous flow and TDI velocities at the
reflectors of qualitative right ventricle function mitral or tricuspid annulus. In the newborn period,
[18,23]. Fractional area change is the method of important changes are seen during the first weeks of
choice for quantitative assessment although it life with a gradual change from a fetal filling pattern
requires further validation in the neonatal popula- (more dependent on atrial contraction) with a
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tion [20 ]. Doppler A more than E wave toward a more mature
The myocardial performance index (MPI) is a filling pattern with an E more than A wave (Fig. 3).
good way to assess both systolic and diastolic func- This is characterized by a progressive increase in E-
tion with normal values in healthy neonates rang- wave velocity and increased E/A ratio. In the new-
ing from 0.25 to 0.38 [24]. The disadvantage of MPI born with high heart rate, E and A waves may be
is that it is nonspecific and influenced by preload fused rendering assessment of diastolic function
and afterload changes, making it of limited use in difficult. Moreover, E-wave velocity is sensitive to
hemodynamically unstable patients. change in preload. Infants with PDA and left-to-
Assessment of diastolic function relies essentially right shunt will exhibit increased pulmonary blood
on a combination of different measurements flow and left atrial pressure resulting in increased
FIGURE 2. Tricuspid annular plane systolic excursion (TAPSE) obtained by M-mode from an apical four-chamber view. Left
picture shows normal TAPSE (22 mm) and right picture abnormal TAPSE (10 mm).
FIGURE 3. TDI obtained from an apical four-chamber view with S0 representing systolic wave, E0 wave representing early
diastolic wave, and A0 wave representing late diastolic wave concomitant to atrial contraction.
mitral E-wave velocity. TDI velocities are routinely quantitative value is not obtained. Unfortunately,
used in adults but have not been well explored in this technique cannot be used in infants with a PDA
the neonate. where the left ventricular output is not anymore a
Assessment of volume status is challenging in surrogate of CO. In those patients, it is proposed to
infants although preload is an important determi- measure the Doppler SVC as a surrogate for left
nant of cardiac output in this population. Echocar- ventricular output. This measurement should be
diographic assessment of preload relies on the done over 5–10 cardiac beats to account for respira-
evaluation of filling pressure. Inferior vena cava tory variation [3].
(IVC) size and collapsibility is the method of choice
to evaluate right heart filling pressure. This can easily
be done in spontaneous breathing infants but utility ECHOCARDIOGRAPHY FOR SUSPECTED
is reduced in ventilated patients. In the presence of PATENT DUCTUS ARTERIOSUS
cardiogenic shock and increased right heart filling Persistent PDA has been suggested as an independent
pressure, the IVC will appear dilated with no respira- risk factor for increased risk of intraventricular hem-
tory variation. Evaluation of left heart filling pressure orrhage, necrotizing enterocolitis, bronchopulmo-
is more complicated but can be qualitatively assessed nary dysplasia (BPD), acute pulmonary hemorrhage
by filling of the left ventricle and measurement of the and carries a 4–8-fold increase in mortality [25,26].
left ventricular end-diastolic dimension but this is The hemodynamic significance of a PDA is not
nonspecific. In infants with a patent foramen ovale directly related to the size of the PDA but depends
(PFO) and left-to-right shunting, mean pressure gra- upon the magnitude of the shunt and the ability of
dient across the PFO gives information on the filling premature myocardium to adapt to this left-to-right
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pressure difference between the left and right atrium. shunt [25,27,28 ,29]. Functional echocardiography
Echocardiographic assessment of cardiac output can help in assessing the hemodynamic repercus-
is a useful adjunct in the evaluation of the hemo- sion of the ductal shunt on pulmonary hyperperfu-
dynamically unstable infant. The most commonly sion and systemic hypoperfusion (Table 2).
used technique uses Doppler estimation of left ven- Ductal size is measured at the narrowest point,
tricular stroke volume, although this technique has usually toward the pulmonary end of the duct where
some problems with reproducibility. The systemic the constriction appears first. Shunt direction
blood flow is obtained by multiplying the time- reflects the pressure difference between the aortic
velocity integral (TVI) obtained by pulsed Doppler and pulmonary artery pressure (PAP) (Fig. 4). Pure
tracing in the left ventricular outflow tract from an left-to-right shunt is seen in infants with low PAP
apical five chambers view by the cross-sectional area and can cause diastolic flow reversal in the descend-
obtained from parasternal long-axis view. Normal ing aorta, mesenteric artery, and cerebral arteries. If
values for left ventricular cardiac index range from PAP is suprasystemic, right-to-left shunt across the
1.7 to 3.5 l/min/m2. Trends in TVI are commonly PDA will occur during systole and more rarely in
used to indicate changes in the cardiac output (CO) diastole. The duration of right-to-left shunt and the
in the unstable NICU patient even if an absolute level of diastolic flow reversal in the descending
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Table 2. Echo parameters suggestive of hemodynamically aorta at the level of the diaphragm is a good
significant PDA reflector on the degree of pulmonary hypertension
and can be used for follow-up. Measurement of
Echo criteria suggestive of
Echo assessment hemodynamically significant PDA
the peak pressure gradient across the PDA may
require continuous-wave Doppler if the velocity
PDA size >2 mm is high.
Left atrium enlargement Left atrium:aorta ratio > 2:1 NPE has also been reported to improve the out-
Left ventricular enlargement LVEDD > Z-score þ2 comes in infants being treated for PDA. Identifying
MPA flow Continuous L-to-R flow from the patients at risk of post-PDA-ligation syndrome
PDA with higher velocity in systole
Turbulent flow
may help in reducing the morbidity and mortality
LPA flow Continuous antegrade flow in diastole
[30]. Similarly, NPE has demonstrated a reduction in
Descending aorta flow Retrograde diastolic flow >30%
number of indomethacin doses used for treating
Middle cerebral and Retrograde diastolic flow
PDA [31,32].
coeliac arteries flow
Left ventricular output >300 ml/min/m2
Transductal flow Peak systolic velocity <1.5 m/s ECHOCARDIOGRAPHIC ASSESSMENT OF
Systolic-to-diastolic velocity PULMONARY ARTERY PRESSURE IN
gradient >4 m/s PERSISTENT PULMONARY
HYPERTENSION OF THE NEWBORN
LPA, left pulmonary artery; LVEDD, left ventricle end-diastolic dimension; MPA,
main pulmonary artery; PDA, patent ductus arteriosus. PPHN is a common problem in critically sick infants
being managed in the NICU and still carries high
FIGURE 4. Patent ductus arteriosus (PDA) shunt direction and velocity (Vmax) allowing for estimation of aorta-to-pulmonary (Ao-PA)
gradient and thus for estimation of pulmonary artery pressure (PAP) and pulmonary hypertension. L–R, left-to-right; R–L, right-to-left.
FIGURE 5. Tricuspid regurgitation jet obtained from an apical four-chamber view and allowing for estimation of systolic
pulmonary artery pressure (SPAP) through the modified Bernoulli equation (SPAP ¼ TRVmax þ RAP).
FIGURE 6. Left ventricle and right ventricle interaction obtained from a parasternal short-axis view showing flattening and
paradoxical motion of the interventricular septum (IVS) during systole with increasing systolic pulmonary artery pressure (SPAP)
and pulmonary hypertension.
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secondary paradoxical septal movement that can diastole, right ventricular free wall collapse during
impair left ventricular contractility and loading con- diastole and respiratory variation of Doppler mitral
ditions [3]. inflow more than 10% and tricuspid inflow more than
The severity of pulmonary hypertension can also 25% are other signs of cardiac tamponade. Distension
be estimated by the direction and velocity of shunt across of the IVC with no respiratory variation is usually also
a PDA but may be limited because of the long and seen and reflects increased right heart filling pressure.
tortuous nature of the duct that renders the Bernoulli
equation not so reliable. A pure right-to-left shunt
across a PDA suggests suprasystemic pulmonary TRAINING AND ACCREDITATION FOR
artery pressure (PAP), whereas a bidirectional trans- NEONATAL FUNCTIONAL
ductal shunt suggests isosystemic PAP (Fig. 4). ECHOCARDIOGRAPHY
The shunt across the PFO is generally bidirec- All the recently published expert consensus state-
tional in the presence of pulmonary hypertension ments have emphasized developing a structured
but can sometimes be left-to-right even in the pres- training program for neonatologists in developing
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ence of severe PPHN. Indeed, the interatrial shunt- echocardiography skills [5,7,8 ,9 ,45]. The varia-
ing depends more on diastolic function of the right tion in such recommendations maybe because of
ventricle. Pure right-to-left shunt across the PFO is the heterogenicity in clinical practice and the dif-
always abnormal and suggests elevated right heart ferent needs across the countries. All the guidelines
filling pressure. A cyanotic CHD should always be have emphasized developing an accreditation pro-
ruled out in the presence of a pure right-to-left cess and developing a robust clinical governance
interatrial shunting. system to improve patient safety.
The pulmonary artery acceleration time (PAAT) to Studies have reported that significant CHD was
right ventricular ejection time (RVET) ratio derived almost always detected on NPE and there is a very
from pulmonary artery Doppler has been shown to low risk of missing underlying significant CHD [39].
negatively correlate with PAP in premature infants. Although this is reassuring, it is important to
PAAT/RVET ratio has been seen to be a good predic- emphasize that the first echocardiography should
tor of late-onset chronic lung disease or BPD [39,40]. always include a comprehensive structural assess-
Other echo parameters such as eccentricity index ment of the heart to rule out major CHD. When the
may be used for qualitative assessment of pulmo- first echocardiography needs to be performed in
nary hypertension. emergency situations where detailed assessment is
NPE is useful in establishment of pulmonary not possible, a comprehensive echocardiography
hypertension and may help in early initiation of should be performed as soon as possible when the
&
pulmonary vasodilator treatment (such as inhaled infant is stable [6 ,7].
nitric oxide) and monitoring the response to treat-
ment. Similarly, early detection of cardiac dysfunc-
tion may help in choosing the appropriate inotropic FUTURE TRENDS
or vasopressor support [41]. TDI is a new technique providing measurements of
myocardial movements and events and may over-
come some of the shortcomings of conventional
ECHOCARDIOGRAPHIC ASSESSMENT OF techniques [46]. Myocardial deformation analysis
PERICARDIAL EFFUSION OR CARDIAC is an emerging quantitative echocardiographic tech-
TAMPONADE nique that allows to characterize global and regional
Pericardial effusion is uncommon in infants treated ventricular function. Cardiac strain is a measure of
in the NICU. It is most often secondary to infusion tissue deformation and strain rate is the rate at
or parenteral nutrition via central line leading to which deformation occurs. These measurements
sudden collapse and unfavorable outcomes have are obtained in neonates using TDI or two-dimen-
been published [42,43]. NPE can be used to diagnose sional speckle tracking echocardiography [47].
pericardial effusion and allows for timely echo- Although promising, these techniques are not used
guided pericardiocentesis [44]. for making bedside clinical decisions in the NICU
The hemodynamic repercussion of pericardial practice and are still used primarily as research tools.
effusion does not depend only on the amount of
pericardial fluid. A large amount of pericardial fluid
can be well tolerated when the fluid accumulates CONCLUSION
slowly and if already present in utero. However, small Bedside functional echocardiography provides real-
but rapidly enlarging pericardial effusion can cause time physiological information and is a useful adjunct
cardiac tamponade. Right atrium collapse at end- to other monitoring tools for critically ill infants. It is
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