Functional Echocardiography in Assessment of the Cardiovascular

System in Asphyxiated Neonates

Martin Kluckow, MBBS, FRACP, PhD

Perinatal asphyxia commonly results in multi-organ damage, and cardiovascular dysfunction is a frequent associ-
ation. Myocardial damage, right ventricular dysfunction, abnormal circulatory transition, and impaired autoregula-
tion may all contribute to postnatal neurological damage. Adequate monitoring and appropriate targeted treatment
therefore are essential after an asphyxial insult. Standard methods of cardiovascular monitoring in the neonate have
limitations. Point of care ultrasound scanning or functional echocardiography offers extra information to assist the
clinician in identifying when there is significant cardiovascular impairment, classifying the underlying abnormal
physiology and potentially targeting appropriate therapy, thereby optimizing the post-insult cerebral blood flow
and oxygen delivery. (J Pediatr 2011;158:e13-8).

T
he neonate with symptoms of perinatal asphyxia usually has a multiorgan insult. The neurological manifestations are
only a part of the underlying pathology. The common clinical appearance of a severely asphyxiated neonatepale,
poorly perfused, and tachycardic despite effective resuscitationsuggests cardiovascular compromise. Involvement
of the cardiovascular system frequently includes primary cardiac dysfunction and circulatory inadequacy, which contributes
to further postnatal neurological injury. After an asphyxial insult, maintenance of tissue oxygenation is a primary aim of man-
agement. Tissue oxygenation depends on oxygen content of the blood, blood flow to the organ, and the tissues ability to extract
and use oxygen. Consequently, cardiac output may be a more important determinant of cerebral blood flow than blood pres-
sure.1 Because cardiac dysfunction is a common outcome of perinatal asphyxia2 and blood pressure is not necessarily reflective
of cardiac output,3 it is important to monitor cardiac output and blood pressure in asphyxiated neonates.
Echocardiography is used for diagnostic purposes in the asphyxiated neonateto rule out primary congenital cardiac dis-
ease, assess neonates with suspected persistent pulmonary hypertension of the newborn (PPHN) and to allow assessment of the
degree of myocardial dysfunction. Echocardiography can contribute to the assessment of myocardial ischemia and dysfunction
because both the electrocardiographic changes and the biochemical changes seen in older children and adults are less common
in neonates.4,5 In adults with acute myocardial injury, two-dimensional echocardiographic measures of cardiac function have
both high positive and negative predictive values of a poor prognosis.6
Traditionally, echocardiographic information is provided in a single consultation by an available cardiologist, with focus on
exclusion of congenital heart disease and PPHN and a current assessment of function. The evolution of the use of point-of-care
functional echocardiography, at the cot side by the clinician caring for the neonate, has resulted in extra hemodynamic data
being available in a timely manner.7,8

Assessment of the Cardiovascular System

Transient myocardial ischemia is a recognized association of perinatal asphyxia, with an incidence from 30% to 82% of severely
asphyxiated neonates.2,9,10 The incidence of myocardial dysfunction may be higher in preterm neonates who already have risk
factors for myocardial impairment because of immaturity of the myocardium.11 Transient myocardial ischemia is often asso-
ciated with evidence of myocardial damage, such as a rise in cardiac troponin levels.12 Diagnosis of myocardial involvement
after a hypoxic ischemic insult can be difficult and requires skills in echocardiography. There are two major patterns of myo-
cardial dysfunction, depression of left ventricular (LV) function assessed with measures of contractility (fractional shortening,
ejection fraction) and reduced cardiac output or aortic valve ejection velocity (Doppler velocity and flow measurements). Re-
duction in cardiac output of asphyxiated neonates is commonly observed.4 The second pattern is moderate to severe pulmonary
hypertension causing tricuspid regurgitation, reduced right ventricular (RV) output, and RV dysfunction.13 In addition to the
impairment of oxygenation that can occur with pulmonary hypertension, there is often an associated reduction in systemic

EF Ejection fraction
FS Fractional shortening
LV Left ventricular From the Department of Obstetrics & Gynecology,
MPI Myocardial performance index University of Sydney, Sydney, Australia

PPHN Persistent pulmonary hypertension of the newborn Please see the Author Disclosures at the end of this
article.
RV Right ventricular
SVC Superior venal cava 0022-3476/$ - see front matter. Copyright 2011 Mosby Inc.
All rights reserved. 10.1016/j.jpeds.2010.11.007

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THE JOURNAL OF PEDIATRICS  www.jpeds.com
blood flow caused by impaired pulmonary venous return to
the left atrium, which compounds the reduced systemic
blood flow from LV dysfunction.
Clinical Assessment
The mainstays of clinical assessment of asphyxiated neonates
have been capillary refill time, acidosis, and blood pressure,
which are all limited in both accuracy of assessment and
the information obtained. Capillary refill time is used in adult
and pediatric intensive care settings as an indicator of poor
perfusion with some correlation;14,15 however, accuracy in
predicting low cardiac output is limited. Similarly, acidosis,
as indicated by lactate level or base deficit, probably reflects
poor perfusion and anaerobic metabolism some hours be-
fore. There is some usefulness in these measures, as shown
by the correlation with important outcomes such as mortal-
ity rate.16 It is generally assumed that normal blood pressure
is indicative of normal cardiac output and thus adequate ce-
rebral blood flow. Several clinical studies have demonstrated
the disconnect between blood pressure and cardiac output
caused by variability of peripheral vascular resistance, partic-
ularly in the newborn.3,17 This is particularly important in the
asphyxiated neonate with a normal systemic blood pressure
but impaired myocardial function and resultant low cardiac
output. With the exception of an impression of impaired
perfusion and later development of acidosis, the only way
to identify these neonates is to also measure cardiac output.
Impaired cardiac output during the immediate post-
asphyxia period may compound the original insult by im-
pairing cerebral hemodynamics as measured with cerebral
blood flow velocities and increased pulsatility/resistance in-
dices. The more significant the cardiac dysfunction, the worse
the outcome in hypoxic-ischemic encephalopathy.18
Qualitative Assessment of Cardiac Function
A simple visual assessment with echocardiography in either
the parasternal long axis or a short-axis parasternal view can
provide significant information about the function of the
myocardium. Visual assessment of contractility is assessed
with the movement of the septum and posterior myocardial
wall and is reasonably accurate for clinicians experienced in
echocardiography.19 Similarly, the filling of the heart can be
assessed by observing the residual volume in diastolethe
LV end diastolic diameter. Generally, severely hypovolemic
neonates will have very little residual cavity in diastole, and
an infant with volume overload will have a significantly in-
creased volume at end diastole. Both of these visual impres-
sions are further quantified with measurement of fractional
shortening, ejection fraction, or the more global function mea-
sures of stroke volume and cardiac output.
M Mode Measurements
M Mode imaging allows measurement of fractional shorten-
ing (FS) and ejection fraction (EF), which are more quantita-
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Vol. 158, No. 2, Suppl. 1
tive measures of the contractility of the ventricles. The
reference range for FS in term neonates is 25% to 40%. EF
is similar to FS, but each of the measures is cubed to allow as-
sessment of volume changes; this also multiples any measure-
ment error, particularly because in the neonate the RV
dominance alters the shape of the ventricles. Other measures
of EF, such as the modified Simpsons rule using biplane
paired echocardiographic apical images in two views, al-
though well validated, are labor intensive and not practical
in sick infants. In a group of asphyxiated neonates, there
was a gradual decrease in the FS with an increasing degree
of asphyxia as determined with Apgar score and low cord
pH level (<7.2).20 Both EF and FS are of limited use in the
neonate because of the presence of higher RV pressure and
consequent reduced septal motion.21 Newer techniques
such as tissue Doppler ultrasound scanning imaging provide
more specific information about regional cardiac function.
Tissue Doppler ultrasound scanning imaging allows
measurement of myocardial velocities and transmyocardial
velocity gradient,22 a potentially useful measure of function,
but there is little data on the use of tissue Doppler ultrasound
scanning imaging in the asphyxiated neonate.
Systolic/Diastolic Time Intervals
Other measures of cardiac function can be determined by
measuring peak velocity, mean acceleration, acceleration
time, and LV ejection time. The systolic time interval ratio
(acceleration time/LV ejection time) was not predictive of
asphyxia.20 Use of more sophisticated measures of contractil-
ity that are independent of preload/afterload, such as the ve-
locity of circumferential shortening or the ratio of velocity of
circumferential shortening to end systolic wall stress, an
afterload adjusted parameter,23 may allow more accurate
assessment of cardiac function in asphyxiated neonates, but
there are few published clinical studies of these measure-
ments in asphyxiated neonates.
Myocardial Performance Index
The myocardial performance index (MPI) combines a measure
of both the systolic and diastolic intervals to characterize global
myocardial performance.24 The MPI is a Doppler ultrasound
scanning-derived index of myocardial performance, combin-
ing the isovolumetric contraction and relaxation time intervals,
used to assess ventricular function. The index is independent of
heart rate and blood pressure and does not rely on geometric
assumptions. Preterm neonates with evidence of mild perinatal
asphyxia (Apgar score 5-7) have an increased MPI compared
with a group of control neonates without evidence of as-
phyxia.25 The index normalized by the third week of life.
Cardiac Output with Doppler Ultrasound
Scanning
A more global assessment of cardiac function can be achieved
by measuring cardiac output non-invasively by using
Kluckow
February 2011
Doppler ultrasound scanning techniques.3,26-29 Ventricular
outputs are measured with two-dimensional echocardiogra-
phy to measure outflow tract diameter and the velocity time
integral.3 The cardiac index is derived by correcting for birth
weight. This Doppler ultrasound scanning-derived non-in-
vasive measure of cardiac output has been well validated
against invasive measures of cardiac output in neonates.28
A reduction in RV output often signifies impaired RV func-
tion. The main source of error is the diameter measurement
of the outflow tractthus a standardized method should be
used and consideration should be given to using a single mea-
sure of diameter for a longitudinal series of measurements.
Similarly attention should be paid to the Doppler ultrasound
scanning angle when measuring velocity to improve accuracy
and repeatability.
Functional echocardiography studies in asphyxiated neo-
nates using these measures have shown reduced LV output
and stroke volume in asphyxiated neonates with non signifi-
cant differences in left ventricular shortening fraction, left
ventricular diameter in systole, left ventricular diameter in
diastole, end systolic wall stress, and peak E/A wave ratio.
These abnormalities in myocardial function were more likely
to be associated with raised markers of myocardial injury,
such as serum cardiac troponin T level.30 It is important to
assess cardiac output in addition to blood pressure because
variations in peripheral resistance in sick neonates mean
that blood pressure and cardiac output are not linearly related.
Superior Venal Caval Flow
Measurement of superior venal cava (SVC) flow has been
used primarily in premature neonates to assess cardiac out-
put independent of the transitional circulation shunts that
result in the actual measured LV and RV output being higher
than the true systemic blood flow. The LV output is increased
by the left-to-right shunt through a patent ductus arteriosus,
and the RV output is increased by the shunt through the
patent foramen ovale.11,31 SVC flow is potentially a proxy
measure for cerebral blood flow,32 and low SVC flow has
been associated with neurological injury in the preterm neo-
nate;33 however, there is no data on the usefulness of this
measure in asphyxiated term neonates. Because SVC flow
represents only a portion of the total venous return to the
heart, it is probably not reflective of the total cardiac output.
Right Ventricular Function
Assessment of the RV function can be achieved with a visual
qualitative assessment of the contractility and filling in
a long-axis view. Paradoxical movement of the septum or
bowing to the left with increased RV pressure can be assessed
in a short-axis view. The pattern of the velocity time ratio in
the RV outflow tract (systolic interval) may also provide
information about RV function and increased pulmonary
pressure, with a reduction in the time to peak velocity as
a proportion of total ejection time34 or even the development
of a biphasic pattern with a mid systolic reduction in velocity.
Functional Echocardiography in Assessment of the Cardiovascular System in Asphyxiated Neonates
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SUPPLEMENT
Very high pulmonary pressures and no ductal off loading are
often associated with very low Doppler ultrasound scanning
velocities and subsequently reduced RV outputs. The modi-
fied Bernoulli equation can be used to estimate the RV pres-
sure by using the gradient across the tricuspid valve when TI
is present.35 Other features of raised RV pressure include in-
creased end diastolic diameter of the right ventricle36 and an
increase in the RV myocardial performance index.37 Another
useful load-dependent measure of ventricular function is the
Doppler ultrasound scanning-derived systolic interval dP/dt
(mm Hg/sec). The velocity of the atrioventricular valve re-
gurgitant jet in a standardized interval represents the rate
of rise of ventricular pressure during isovolumetric contrac-
tion. dP/dt is reduced with decreasing ventricular function
(normal >1000 mm Hg/sec).
In normal physiological states without the use of positive
pressure ventilation, the pulmonary blood flow and venous re-
turn to the left side of the heart is promoted by spontaneous
breathing and negative intrathoracic pressure. RV systolic func-
tion when pulmonary vascular resistance is low is not essential.
In the case of an asphyxiated neonate requiring mechanical
ventilation or high frequency oscillatory ventilation with
a high mean airway pressure, normal RV function is critical
for pulmonary blood flow, often against increased pulmonary
vascular resistance. Impaired pulmonary blood flow reduces
LV preload, interfering with LV function potentially reducing
systemic blood flow and subsequently cerebral oxygen delivery.
Assessment of Volume Status/Fluid
Responsiveness
Both hypotension and impaired cardiac output are common
outcomes of asphyxial damage to the myocardium, and use
of volume resuscitation in the setting of asphyxia is common.
Volume is critical when there is evidence of hypovolemia or
an acute change in the systemic vascular resistance resulting
in vasodilation of the peripheral vasculature. Volume is also
an important adjunct to the use of inotropes. Volume in-
creases cardiac output in sick term neonates by increasing
stroke volume rather than heart rate or contractility.38 Para-
doxically, excessive volume administration in the setting of
myocardial impairment can result in volume overload,
worsening of oxygenation, and congestive cardiac failure.
Accordingly, assessment of volume status and in particular
the concept of fluid responsiveness is potentially impor-
tant in the treatment of an asphyxiated neonate.
Previously, fluid responsiveness was assessed by using
filling pressures and a test fluid challenge, but increasingly
echocardiography is being used in older children and adults
to assess volume status to guide volume therapy. Fluid
responsiveness refers to the prediction that volume therapy
will result in an increase in cardiac output.39 The usefulness
of assessment of the effect of the respiratory cycle on cardiac
function to predict fluid responsiveness has been demon-
strated in adults.39 The most useful measurement was the
collapsibility index of the SVC, a measurement of the cyclic
changes in SVC diameter induced by the application of
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positive pressure with mechanical ventilation. Assessments of
changes in the distensibility of the inferior vena cava have
also been used in neonates as a measure of fluid responsive-
ness, although with less reliability than in adults.40
Distinguishing the normovolemic neonate with asphyxia
shock from a truly hypovolemic neonate is clinically
important, particularly with asphyxia in which impaired
myocardial function means that excessive volume is not indi-
cated.41 Asphyxiated neonates often received volume therapy
because of a failure to respond to resuscitation rather than
clinically suspected hypovolemia. The common outcome of
excessive volume administered in the setting of myocardial
dysfunction is fluid overload and further impairment of gas
exchange. Functional echocardiography is potentially able
to allow targeting of the appropriate amount of volume
and avoid this added complication in asphyxia.
Pulmonary Hypertension
Raised pulmonary pressures and PPHN are common compli-
cations of perinatal asphyxia, but the role of functional
echocardiography in this area is also critically important.
PPHN is a multifactorial dynamic process, and the treatment
of asphyxiated neonates is assisted greatly by understanding
the underlying physiology, particularly as the clinical situa-
tion changes.34,42 The components of this include measures
of myocardial and ventricular output (particularly right
sided), various echocardiographic measures of pulmonary
pressure as aforementioned, and assessment of patency and
direction of shunt in the patent ductus arteriosus. All these
measures are well suited to functional echocardiography
undertaken by the clinician at the bedside.43
Many of the therapies used during the management of
pulmonary hypertension can be monitored with functional
echocardiography. Adequacy of volume resuscitation, the
effect of different inotropes on the contractility, cardiac
output, and degree of systemic to pulmonary shunt are all
easily assessed with ultrasound scanning. The course of raised
pulmonary pressure is variable in different infants and is not
always congruent with the clinical presentation.34,42 Regular
functional echocardiography allows timely identification of
changes in the underlying physiology and subsequent
alteration in management, sometimes earlier than when
only clinical signs and monitoring are used. Evidence of
pulmonary hypertension as demonstrated with high velocity
tricuspid regurgitation is more common in neonates with
clinical asphyxia (38.5% versus 11.4% in a non-asphyxiated
group of neonates).13
Therapeutic Hypothermia and
Cardiovascular Function
With the use of therapeutic hypothermia for the manage-
ment of perinatal asphyxia, there is a lack of information
on the effect of cooling on cardiac function and hemodynamics.
This is likely to be particularly relevant during whole body
cooling. Hypotension and sinus bradycardia are adverse
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Vol. 158, No. 2, Suppl. 1
effects of cooling that have been consistently noted.44 More
recently, significantly decreased LV cardiac output (67% of
post-hypothermic range) was demonstrated during thera-
peutic cooling, with a consistent increase occurring during
re-warming. Despite this significantly decreased cardiac
output, there were no differences in systemic blood pressure,
signifying compensatory adjustments in systemic vascular
resistance. The increase in cardiac output appeared to be
mediated by an increase in contractility rather than the
re-warming process.45 This study also demonstrates the im-
portance of assessing cardiac output in asphyxiated cooled
neonates because systemic blood pressure was not signifi-
cantly different in groups. This is particularly important
in asphyxiated neonates who may also have impaired
autoregulation, rendering the cerebral blood flow even
more dependent on maintenance of cardiac output and
blood pressure. It is unclear whether the apparent physiolog-
ical reduction in cardiac output in some neonates during
therapeutic hypothermia is acceptable for the ongoing risk
of further brain injury.
Training in Functional Echocardiography
The usefulness of bedside functional echocardiography is
high in the setting of perinatal asphyxia. Bedside functional
echocardiography has become an important tool in the treat-
ment of critically ill intensive care patients in both adult and
pediatric intensive care units,46 permitting rapid and precise
diagnosis and longitudinal assessment of hemodynamic
function. Increasingly the role of functional echocardiogra-
phy in the neonatal unit has also been recognized.8,47,48
The expertise of a consultational cardiologist is important
for a high level scan to exclude structural heart disease and
to provide baseline functional information. The bedside cli-
nician who is acutely aware of the clinical course and treat-
ment of the patient can perform longitudinal functional
studies when they are important for clinical decision-making.
As the role and usefulness of functional echocardiography
develops in the neonatal intensive care unit, ways to
introduce this skill to nurseries and train and accredit clini-
cians will become increasingly important.49 In neonatology,
the process of development of appropriate training and
accreditation has been impeded by poor acceptance by
traditional consultative groups, including cardiologists and
radiologists. Some countries have introduced a more formal
certification process and have developed a centralized train-
ing curriculum.50
Conclusion
Perinatal asphyxia commonly results in multiorgan damage
and cardiovascular dysfunction. Myocardial damage, RV
dysfunction, abnormal circulatory transition, and impaired
autoregulation may all contribute to postnatal neurological
damage. Adequate monitoring and appropriate targeted
treatment are essential components of the intensive care of
an asphyxial insult. Because standard methods of monitoring
Kluckow
February 2011
have limitations in assessing cardiovascular adequacy, func-
tional echocardiography offers extra information to assist
the clinician in identifying when there is significant cardio-
vascular impairment, classifying the underlying abnormal
physiology, and potentially targeting appropriate therapy,
thereby optimizing the cerebral blood flow and oxygen deliv-
ery after insult. n
Author Disclosures
Martin Kluckow, MBBS, FRACP, PhD, has no financial ar-
rangement or affiliation with a corporate organization or
a manufacturer of a product discussed in this supplement.
Reprint requests: Dr.Martin Kluckow, MBBS, FRACP, PhD, University of
Sydney, Department of Obstetrics & Gynecology, Sydney 2065, Australia.
E-mail: mkluckow@med.usyd.edu.au
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