Paediatrica Indonesiana
VOLUME 49
Original Article
Echocardiographic patterns in asphyxiated neonates
Maswin Masyhur, Idham Amir, Sukman Tulus Putra, Alan Roland Tumbelaka
Abstract
Background Neonatal asphyxia is a disorder in neonates due
to decreased oxygenation (hypoxia) and decreased perfusion to
organs (ischemia). Duration of asphyxia and early management
influence the severity of organ dysfunction, including the heart.
Objectives To obtain patterns of cardiac abnormality in
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echocardiography.
Design $FURVVVHFWLRQDOVWXG\ZDVSHUIRUPHGRQDVSK\[LDWHG
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Results 7KHUH ZHUH  DVSK\[LDWHG QHRQDWHV DQG  QRQ
July ‡ NUMBER 4
incidence in developing countries is higher than in
developed countries due to inadequate antenatal
care. Most of these asphyxiated neonates do not
receive appropriate management, resulting in high
mortality rate. :LWK DVSK\[LD LQFLGHQFH RI 
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born each year.,Q'HSDUWPHQWRI&KLOG+HDOWK&LSWR
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with severe asphyxia.4
Neonatal asphyxia is a disorder due to decreased
oxygenation (hypoxia) and decreased perfusion to
organs (ischemia).5,6 In asphyxia state, fetal oxygen
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common cardiac abnormality found in asphyxiated neonates was
patent ductus arteriosus, followed by atrial septal defect, tricuspid
regurgitation, and pulmonary hypertension.
Conclusion &DUGLDFDEQRUPDOLW\LVVLJQLILFDQWO\IRXQGPRUHRIWHQ
LQ DVSK\[LDWHG WKDQ LQ QRQDVSK\[LDWHG QHRQDWHV [Paediatr
Indones. 2009;49:214-18].
Keywords: neonatal asphyxia, heart disease,
echocardiography
N
eonatal asphyxia is still one of the most
common cause of mortality and morbidity
in developed and developing countries,
including in Indonesia. The incidence
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depends on gestational age and birth weight. The
214‡Paediatr Indones, Vol. 49, No. 4, July 2009
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oxygen and carbon dioxide interchange in main tissue
and organs are also decreased. These conditions
result in hypoxemia, accumulation of carbon dioxide,
decreased blood pH, and furthermore those will
influence various organs, including the heart. Organ
dysfunction in asphyxiated neonate depends on
duration of asphyxia and early management.Studies
on neonatal asphyxia show organ damage in many of
them. Asphyxiated infants experience blood flow
redistribution which provides the heart with more
blood flow than other organs. Therefore the heart
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 Maswin Masyhur et al: Echocardiographic patterns in asphyxiated neonates
LV UHODWLYHO\ UHVLVWDQW WR K\SR[LD11 however many
cardiac abnormality have been observed in neonates
with asphyxia. We performed a pilot study to
determine cardiac status in neonates with asphyxia.
Methods
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the first minute for asphyxiated group, and term
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congenital malformation, neonates born to mothers
who suffered from intrauterine infection, inadequate
antenatal care, incomplete data, and disapproval from
parents or surrogates.
Newborns who met the inclusion criteria
underwent several examinations: anthropometry
(birth weight and birth length), gestational age
(Ballard score), and physical examination, particularly
Results
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gestational age, sex, and birth methods are shown in
Table 1.
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neonates. The means of birth weight in both groups
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asphyxiated neonates respectively.
In heart rate examinations, neither bradycardia
nor tachycardia was found in both groups. Murmur was
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neonates were with severe asphyxia, and two neonates
with moderate asphyxia. There were no neonates with
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In echocardiography examination, cardiac
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neonates. This value show significant difference
proportion between the two groups using Fisher test,
with P YDOXHRIFRQILGHQFHLQWHUYDORI
heart rate and heart examinations. Echocardiography
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University of Indonesia was obtained.
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severe asphyxia group (4 out of 9 neonates) rather
than in mild or moderate asphyxia group (Table 3).
This study found that small PDA occurred more
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Table 1. Subjects’ characteristics
no small PDA was found in severe asphyxia group.
Asphyxia Non-asphyxia
n = 22 n = 22
Moderate PDA was found in four neonates in severe
Sex Male 8 14 DVSK\[LD JURXS  QHRQDWHV LQ PRGHUDWH DVSK\[LD
Female 14 8 JURXSDQGQRQHLQQRQDVSK\[LDJURXS
Gestational age 37 weeks 4 2
38 weeks 8 11
39 weeks 1 2
Discussion
40 weeks 9 7
Birth methods Spontaneous 7 10
Cesarean This was a cross sectional study using convenient
14 10
section sampling method due to time limitation. Most
Vacuum
1 2
epidemiology studies need larger subjects, while this
extraction
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Table 2. Cardiac abnormality detected with echocardiography

Cardiac abnormality Asphyxia Non-asphyxia
n = 22 n = 22 P 95%CI
Yes 7 1 0.023 1.33 to 3.33
No 15 21 PR: 2.1

Paediatr Indones, Vol. 49, No. 4, July 2009‡215

 Maswin Masyhur et al: Echocardiographic patterns in asphyxiated neonates

Table 3. Cardiac abnormality and severity of asphyxia

Non – asphyxia Asphyxia (n = 22)
Echocardiography results (n = 22) Moderate asphyxia Severe asphyxia
(n = 13) (n = 9)
Normal 21 10 5
Abnormal 1 3 4

Moderate PDA - - 1
Moderate PDA + small ASD + moderate TR - 1 -
Moderate PDA + small ASD + PH - - 1
Moderate PDA + PFO - 1 -
Moderate PDA + mild TR + PH - - 1
Moderate PDA + TR + PFO - - 1
PFO + TR - 1 -
VSD 1 - -

PDA : Patent ductus arteriosus, ASD: Atrial septal defect, VSD: Ventricular septal defect,
PFO: Patent foramen ovale, TR: Tricuspid regurgitation, PH: Pulmonary hypertension

done to reduce bias. In this study female predominance alIRXQGWKDWWKHPXUPXULQDVSK\[LDEDELHVZDV

occurred in asphyxia group, while male predominance more frequent than this study. The possible reason is
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influence the incidence of asphyxia. The incidence of
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incidences of patent ductus arteriosus (PDA) and atrial
septal defect (ASD) are higher in female.14
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In asphyxia babies, acute hypoxia redistributes blood
flow so that the heart will receive more blood compared
to other organs.11 These changes is happened due to
brain and heart vascular resistance reduction.9
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were lower than previous study done by Karimi et al15 UHVXOW LV  ORZHU WKDQ VWXG\ FRQGXFWHG E\ /RZ et
ZKRIRXQGWKDWWKHPHDQVRIELUWKZHLJKWZHUH al. These differences might be caused by the variation
6'  JUDP IRU DVSK\[LD JURXS DQG  6' of asphyxia criteria and sample. Definition of asphyxia
JUDPIRUQRQDVSK\[LDJURXS7KHGLIIHUHQFH in this study was based on Apgar score while in study
is due to higher gestational age in study by Ercan et conducted by Low et al was based on umbilical pH with
al156'DQG6'FRPSDUHGWR EDVHH[FHVVRIPRUHWKDQPPRODQGPHDQS+RI
WKLVVWXG\6'DQG6' Ancel The degree of asphyxia in study conducted by Low et al
et al16 reported that mean birth weight for asphyxia was more severe therefore more cardiac abnormalities
EDELHVZDV6'JUDP Mean birth weight were found. The higher probability of having cardiac
in study done by Low et al is lower compared to abnormalities in that study was due to prematurity.
these studies, because of lower gestational age (mean The frequency of cardiac abnormalities in this
ZHHNV )RXUWHHQRXWRIEDELHVLQWKLVVWXG\ study was lower than many studies, i.e. in studies
were delivered by caesarean section. This result is in FRQGXFWHGE\&KLVWRSKHUet al%DUEHULet al
accordance with study by Ancel et al16RXWRI DQG+DQNLQVet alKRZHYHULWLVLQ
babies). Some literatures also reported that caesarean
section is a risk factor for asphyxia.
In this study, murmur was found in six
asphyxia babies with moderate PDA, while none was
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that murmur in neonates with left to right shunt is
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216‡Paediatr Indones, Vol. 49, No. 4, July 2009
contrast with study conducted by Martin et al16
This difference is due to difference of design, sample
size, and subject’s characters such as inclusion criteria,
instruments, and asphyxia criteria.
There is significant difference of subject
proportion of having cardiac abnormalities between
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 Maswin Masyhur et al: Echocardiographic patterns in asphyxiated neonates

RI&,WRDQGSUHYDOHQFHUDWLR Penanganan mutakhir bayi prematur: Memenuhi kebutuhan

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This study shows the most frequent cardiac
abnormalities found in asphyxia newborns is PDA
bayi prematur untuk menunjang peningkatan kwalitas
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Harliany E, Sofiatin Y, et al. Management of birth asphyxia at
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study conducted by Herdy et alLQDVSK\[LD
newborns). Deselina et al  reported the higher
incidence of PDA (seven in 11 preterm asphyxia
newborns).
PDA closure physiologically happens in the
second day until fourth day of life. The conditions that
inhibit PDA closure are asphyxia, low birth weight
and prematurity.193'$ZLWKGLDPHWHUOHVVWKDQPP
is classified as small. In this study this condition is
classified as normal because echocardiography were
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correlations in postasphyxial organ damage: A donor organ
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4. Manoe VM, Amir I. Gangguan fungsi multi organ pada
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MD, Eyal FG, Zenk KE, editors. Neonatology management,
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6. Report of the National Neonatal Perinatal Database (National
performed in first and second day of life in which
normal closure has not occurred yet. Reller et al
reported that prevalence of PDA closure in the fourth
GD\ZDVZKLOH(YDQDQG$UFHO reported that
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Tricuspid insufficiency is a cardiac abnormality
characterized by right ventricle to right atrium blood
flow during systolic phase. Tricuspid insufficiency
in asphyxia is due to hypoxia that damages the
papillary muscle and tricuspid annulus. Tricuspid
insufficiency was found in two out of nine babies with
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asphyxia, and none found in non asphyxia babies.
This result was lower that study done by Barberi et al
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Stark AR, penyunting. Manual of neonatal care. 4th ed.
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QRQDVSK\[LDEDELHV+HUG\et al reported that six
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which was lower than this study. These differences are
probably caused by different asphyxia definition and
degree in research subject.
In conclusion, cardiac abnormality is significantly
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asphyxiated neonates.
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 Maswin Masyhur et al: Echocardiographic patterns in asphyxiated neonates
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