A C TA Obstetricia et Gynecologica

AOGS M A I N R E SE A RC H A R TI C LE

Fetal aortic isthmus Doppler measurements for prediction

of perinatal morbidity and mortality associated with fetal
growth restriction
€ UR
KHALIL ABDELRAZZAQ, AHMET OZG € YENIEL*, AHMET METE ERGENOGLU, NURI YILDIRIM,
FUAT AKERCAN & NEDIM KARADADASß
Department of Obstetrics and Gynecology, Faculty of Medicine, Ege University, Bornova, Turkey

Key words Abstract

Aortic isthmus, fetal acidosis, fetal blood
flow, fetal growth restriction, perinatal
outcome
Correspondence
€ u
Ahmet Ozg €r Yeniel, Department of
Obstetrics and Gynecology, Faculty of
Medicine, Ege University, Bornova, TR-35100
Izmir, Turkey. E-mail: drayeniel@hotmail.com
Conflict of interest
The authors have stated explicitly that there
are no conflicts of interest in connection with
this article The authors alone are responsible
for the content and writing of the paper.
Please cite this article as: Abdelrazzaq K,
€ Ergenoglu AM, Yildirim N,
Yeniel AO,
Akercan F, Karadadasß N. Fetal aortic isthmus
Doppler measurements for prediction of
perinatal morbidity and mortality associated
with fetal growth restriction. Acta Obstet
Gynecol Scand 2013; 92:656–661.
Objective. To identify the role of longitudinal measurements of fetal aortic isth-
mus blood flow using Doppler ultrasonography in the prediction of perinatal
morbidity and mortality. Setting. Obstetrics department of a university hospi-
tal. Population and design. This prospective study includes women with fetal
growth restriction and abnormal umbilical artery Doppler results, seen between
November 2009 and January 2011. Methods. 31 women were divided into two
groups according to the aortic isthmus blood flow pattern just before birth:
anterograde (n = 12) or retrograde (n = 19). Main outcome measure. Longitu-
dinal measurements of fetal aortic isthmus in relation to perinatal outcome.
Results. Total morbidity and mortality rates were significantly higher in the ret-
rograde flow group. There was no statistically significant difference for respira-
tory distress syndrome, intraventricular hemorrhage, bronchopulmonary
dysplasia or necrotizing enterocolitis, but the neonatal sepsis rate was signifi-
cantly higher in the retrograde flow group. An abnormal aortic isthmus flow
pattern was detected approximately 15–20 days after umbilical artery and mid-
dle cerebral artery Doppler flow abnormalities and 3–7 days before deteriora-
tion in ductus venosus blood flow. Conclusion. We suggest that aortic isthmus
Doppler measurements are useful for identifying fetal growth restriction before
deterioration in ductus venosus blood flow and fetal acidosis.

Received: 1 January 2012 Abbreviations: AI, aortic isthmus; BPD, bronchopulmonary displasia; DV,
Accepted: 4 December 2012 ductus venosus; FGR, fetal growth restriction; IFI, isthmic flow index; IVH,
intraventricular hemorrhage; MCA, middle cerebral artery; NEC, necrotizing
DOI: 10.1111/aogs.12070 enterocolitis; PI, pulsatility index; RDS, respiratory distress syndrome; UA,
umbilical artery.

deaths and 10% of perinatal deaths are related to

FGR (3).
Introduction
Fetal growth restriction (FGR), which is a type of “intra-
uterine programming defect,” may be an important pre-
dictor of adverse perinatal outcomes and long-term Key Message
sequelae, such as cerebral palsy and metabolic diseases of Aortic isthmus Doppler measurements are useful for
adulthood (1). FGR is one of the most important causes identifying fetal growth restriction before deteriora-
of perinatal morbidity and mortality and is associated tion in ductus venosus blood flow and fetal acidosis
with chronic diseases such as diabetes mellitus and car- occur.
diovascular disease (2). Fifty-two percent of intrauterine

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656 Acta Obstetricia et Gynecologica Scandinavica ª 2013 Nordic Federation of Societies of Obstetrics and Gynecology 92 (2013) 656–661
K. Abdelrazzaq et al.
The aim of perinatal care must be both to provide
appropriate patient follow-up and to determine the opti-
mal time for intervention to prevent permanent damage
in FGR fetuses. Because there is no effective intrauterine
treatment for this condition, clinical management focuses
on the proper timing of delivery to prevent fetal acidosis
or demise (4). The most important independent risk fac-
tor for an adverse perinatal outcome is gestational age,
especially before 32–34 weeks, when the risk is higher (5).
There are many invasive and noninvasive methods to
detect the problems in utero-placental, umbilical blood
flow or fetal circulation. Doppler sonography is one of
the most common methods used for this purpose. It is
noninvasive, easy and repeatable. Doppler sonography
helps with diagnosing FGR correctly and improves fetal
outcomes by guiding the correct timing for birth (6).
Progressive deterioration in Doppler findings is related to
perinatal morbidity and mortality in preterm fetuses with
FGR. The most important factor affecting the neonatal
morbidity is gestational age. However, fetal distress indi-
cators, such as abnormal Doppler findings, are also asso-
ciated with stillbirth and fetal acidemia. Therefore,
arterial and venous Doppler should be performed in pre-
term fetuses with FGR (7).
The aortic isthmus (AI) is the portion of the aorta
between the origin of the left subclavian artery and that of
the intersection point of the ductus arteriosus and
descending aorta; it marks the partial separation of fetal
blood flow derived from the right and left ventricles. AI
blood flow represents the output flow of both ventricles
and the difference of placental and cerebral blood flow
resistance. The AI is the only arterial connection between
the right ventricle, which mainly supplies the systemic and
placental circulation, and the left ventricle, essentially cor-
responding to the cerebral vascular network. Conse-
quently, its blood flow pattern reflects the balance between
both ventricular outputs and the differences in the imped-
ance of both vascular systems. Thus, it helps to predict
perinatal morbidity and mortality (8–10). In this study,
we aimed to identify the role of fetal AI Doppler measure-
ments to predict perinatal morbidity and mortality.
Material and methods
A total of 31 patients between 24 and 37 weeks of gesta-
tion were seen between November 2009 and January 2011
at the Ege University Hospital with the diagnosis of FGR.
The study design was accepted by the Ethics Committee
of Ege University. All sonographic results were recorded
and evaluated prospectively. Exclusion criteria were nor-
mal umbilical artery (UA) Doppler flow, fetal anomaly,
chromosomal anomaly, fetal infection, multiple pregnancy
and premature rupture of membranes.
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Acta Obstetricia et Gynecologica Scandinavica ª 2013 Nordic Federation of Societies of Obstetrics and Gynecology 92 (2013) 656–661
Fetal aortic isthmus flow and growth restriction
The isthmic flow index (IFI) is calculated using the fol-
lowing formula: IFI = (S + D)/S (11) where S and D are,
respectively, the systolic and diastolic Doppler blood flow
velocity integrals. If IFI is  1, the flow is anterograde,
and if IFI is <1, the flow is retrograde. In this study,
patients were divided into two groups according to the
AI Doppler measurements just before birth: anterograde
(n = 12) or retrograde (n = 19). To detect the progres-
sion of arterial and venous Doppler parameters, patients
were evaluated by Doppler at least twice at certain inter-
vals by the first and second author together. The Voluson
E8 Doppler Sonography device (GE Healthcare, Milwau-
kee, WI, USA) was used for sonographic examinations
and measurements. In all cases, sonographers were able to
record the AI flow. The clinician managing the pregnancy
was not informed about AI Doppler findings.
Fetal gestational age was calculated according to the
maternal last menstrual period and confirmed by first tri-
mester ultrasound crown-rump length. If the difference
between crown-rump length and last menstrual period
was more than seven days, the crown-rump length calcu-
lation was accepted as the gestational age.
Estimated fetal weight was calculated using the bipari-
etal diameter, abdominal circumference and femur length
measurements as observed by ultrasound. Estimated fetal
weight <10th percentile for gestational age was considered
equivalent with FGR, and this diagnosis was confirmed
after birth.
UA, middle cerebral artery (MCA), AI and ductus
venosus (DV) Doppler measurements were performed.
All measurements were performed in the supine and left
lateral tilt position, but not during fetal movement, fetal
respiration or uterine contractions. The AI Doppler mea-
surement was performed using the longitudinal aortic
arch or three-vessel and trachea section with an inson-
ation angle of <30°.
An MCA pulsatility index (PI) of <5th percentile for
gestational age was considered a brain sparing effect. If
IFI was <1, the flow was considered retrograde (abnor-
mal). An absent or reverse “a wave” at the DV was
accepted as abnormal DV blood flow.
Since the normal distribution of Doppler indices
changes with gestational age, individual measurements
were normalized for statistical analysis by converting
measurements into Z-scores (standard deviation from the
gestational age mean), based on our measurements.
Between the first examination and delivery, the deteriora-
tion observed for Doppler criteria (non-linear regression
analysis) was recorded and regression curve analysis of
Z-scores for each parameter performed.
Arterial blood samples were obtained from the umbili-
cal cord just after birth before placental delivery. The
blood sample pH was assayed using the Nova Biomedical
657
Fetal aortic isthmus flow and growth restriction K. Abdelrazzaq et al.

(Nova Biomedical, Waltham, MA, USA) device, and if intrauterine death were higher in the retrograde flow
the pH was <7.1, the fetus was considered to be acidotic. group. Apgar scores at five minutes were significantly
Decision on delivery was made when the reverse “a higher in the anterograde flow group than other groups.
wave” at the DV Doppler was seen, but if there was any There was no significant difference in the mode of deliv-
other fetal distress sign such as late decelerations on the ery, birthweight, sex or UA pH. Neonatal morbidity and
non-stress test, the patient was taken to the delivery room. mortality rates are compared in Table 1. Total morbidity
The main outcomes of this study were maternal and and mortality rates were significantly higher in the retro-
gestational age, birthweight, five-minute Apgar score, grade flow group. There were no significant differences as
birth method, UA pH at birth, intrauterine death, neona- regards RDS, IVH, BPD and NEC, but neonatal sepsis
tal death, need for care within the neonatal intensive care was significantly higher in the retrograde flow group.
unit and complications of preterm birth, such as respira- Retrograde AI flow has a higher sensitivity for total
tory distress syndrome (RDS), intraventricular hemor- morbidity and mortality than UA flow absent or reversed
rhage (IVH), bronchopulmonary dysplasia (BPD), end-diastolic flow velocity, MCA PI, DV absent or
necrotizing enterocolitis (NEC) and neonatal sepsis. reversed end-diastolic flow velocity, AI PI and delivery
AI anterograde and retrograde flows were evaluated before 28 weeks of gestation (Table 2).
with Pearson’s chi-squared or Fisher’s exact test for the Without knowledge of the AI flow pattern, the patients
categorical variables and Mann–Whitney U test for the were divided into three groups to investigate the role of
numeric variables. Z-scores were calculated for UA PI, AI PI, resistance index, end-diastolic velocity, peak sys-
MCA PI and AI PI; non-linear regression analysis was tolic velocity and time-averaged maximum velocity:
performed for the regression curve analysis of Z-scores fetuses with and without complications from prematurity,
for each parameter. The predictive value of the AI and and fetuses who died (intrauterine or neonatal). There
other Doppler variables in predicting morbidity and mor- was a significant relationship between AI PI, AI resistance
tality was assessed by estimation of sensitivity, specificity, index, AI end-diastolic velocity and the complication risk
predictive values and likelihood ratios. Odds ratios and a (Figure 1). The relation between the complication risk
confidence interval of 95% with significance at p < 0.05 and AI peak systolic velocity and time-averaged maxi-
were used. SPSS 18.0 for Windows (SPSS Inc., Chicago, mum velocity was not significant.
IL, USA) was used to complete the statistical analysis. The progression of Doppler parameters in serial exam-
inations is shown in Figure 2. Between the first examina-
tion and delivery, significant deterioration was observed
Results
The women were divided into two groups according to Table 1. Neonatal morbidity and mortality rates among fetuses by
their AI blood flow pattern just before birth, either aortic isthmus (AI) flow direction.
anterograde (n = 12) or retrograde (n = 19). In nine of
Anterograde Retrograde
19 patients AI flow patterns were anterograde at hospital-
AI flow AI flow
ization but retrograde at follow-up. In both the antero-
grade and retrograde groups the average maternal age was n (%) n (%) p
29 years. Preeclampsia was detected in six of 12 patients
Total morbidity 1 9.1 9 47.4 0.049
in the anterograde group and nine of 19 in the retrograde Respiratory 1 9.1 5 26.3 0.372
group. There was oligohydramnios in eight of the 12 and distress
10 of the 19 patients in the anterograde and retrograde syndrome
groups, respectively. Gestational age at time of hospital- Intraventricular 0 0.0 1 5.3 1.000
ization was 33 weeks (range 26–35) in the anterograde hemorrhage
(Grade III–IV)
group and 28 weeks (range 24–36) in the retrograde
Bronchopulmonary 0 0.0 1 5.3 1.000
group. The gestational age at birth was 35 weeks (range 3
dysplasia
–36) in the anterograde group and 32 (range 25–37) Necrotizing 0 0.0 2 10.5 0.520
weeks in the retrograde group. The gestational age both enterocolitis
at hospitalization and at birth was significantly lower in Sepsis 0 0.0 8 42.1 0.014
the retrograde group (p = 0.016 and 0.017, respectively). NICU stay >14 6 4.5 9 47.4 1.000
There was no significant difference between the two days
Total mortality 0 0.0 7 36.8 0.029
groups in terms of maternal age, preeclampsia rate, or
In utero 0 0.0 4 21.1 0.268
oligohydramnios.
Neonatal death 0 0.0 3 15.8 0.279
There was no significant difference between the two
groups for birth indication, but placental abruption and NICU, neonatal intensive care unit.

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658 Acta Obstetricia et Gynecologica Scandinavica ª 2013 Nordic Federation of Societies of Obstetrics and Gynecology 92 (2013) 656–661
K. Abdelrazzaq et al. Fetal aortic isthmus flow and growth restriction

Table 2. Sensitivity, specificity, positive predictive value (PPV),

negative predictive value (NPV) and likelihood ratio (LR) for morbidity
and mortality of the last Doppler examination in different vessels.

Sensitivity Specificity PPV NPV

(%) (%) (%) (%) LR+

Total morbidity
UA AREDV 20 85 40 68 1.33
MCA PI 90 20 36 43 1.12
DV AREDV 30 70 33 66 1.00
Retrograde AI flow 90 50 47 90 1.80
AI PI 60 65 46 76 1.71
Birth before 28th – 85 – 63 –
weeks
Total mortality
UA AREDV 42 91 60 84 4.9 Figure 2. Z-scores of Doppler parameters during the days before
MCA PI 71 13 20 60 0.82 birth. ▲: umbilical artery pulsatility index (PI), ■: middle cerebral
DV AREDV 42 73 33 81 1.6 artery PI, Δ: aortic isthmus PI, □: ductus venosus PI.
Retrograde AI flow 100 47 36 100 1.9
AI PI 57 60 30 82 1.4
Birth before 28th 42 100 100 85 – outcomes, as documented by previous studies (9,10).
weeks
Total morbidity and mortality rates were significantly
AI PI, aortic isthmus pulsatility index; DV AREDV, ductus venosus higher in the retrograde flow group. Although total mor-
absent or reversed end diastolic-flow velocity; MCA PI, middle cere- bidity is found to be higher in the retrograde flow group,
bral artery pulsatility index; UA AREDV, umbilical artery absent or only neonatal sepsis has a significant relationship with
reversed end diastolic-flow velocity. abnormal AI flow, whereas RDS, IVH, BPD nor NEC had
no association. According to our study, AI PI and AI
resistance index values were significantly associated with
perinatal complications and fetal death. We detected an
abnormal AI flow pattern approximately 15–20 days after
UA and MCA Doppler flow abnormalities and 3–7 days
before deterioration in DV blood flow. These data suggest
that retrograde flow in the AI indicates fetal acidosis
before the abnormal flow pattern in the DV. Doppler
sonography cannot be used as a screening test (12) in
fetuses with FGR; however, a meta-analysis showed that
perinatal morbidity has decreased in 38% of these preg-
nancies (6).
Gestational age at birth is an independent risk factor
for neonatal outcomes and may increase fetal and neona-
tal mortality (13). Each intrauterine day increases the
Figure 1. The distribution of aortic isthmus end diastolic values by chance of survival by 2% until the 28th week of preg-
gestational age and according to 5th, 50th and 95th percentile with
nancy (14). In a study that included 33 severe, early-onset
perinatal outcomes. AoI-EDV, Aortic isthmus end diastolic velocity;
FGR fetuses, the poor perinatal outcome ratio was 45%
IUMF, in utero mort-fetus.
and perinatal mortality 36% in patients who gave birth
before 30 weeks of pregnancy (15). There are also differ-
for Doppler criteria (non-linear regression analysis). ent outcome ratios in different studies. Brodszki et al.
According to the data, retrograde AI flow was detected (16) reported that the survival rate of live-born infants
approximately 15–20 days after abnormal UA and MCA up to two years of age was 90% among fetuses with
flows and 3–7 days before an abnormal DV flow pattern. absent or reversed end diastolic-flow velocity in the UA
and growth restriction, delivered on fetal indication
before 30 gestational weeks.
Discussion
In the case of absent or reversed UA end-diastolic flow
Our study confirms that there is a strong association velocity, perinatal mortality risk increases four- to 10-fold
between retrograde flow in the AI and adverse perinatal in fetuses with FGR (17). According to another study,

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Acta Obstetricia et Gynecologica Scandinavica ª 2013 Nordic Federation of Societies of Obstetrics and Gynecology 92 (2013) 656–661 659
Fetal aortic isthmus flow and growth restriction
abnormal uterine artery blood flow with abnormal UA
Doppler parameters worsens the perinatal outcome (18).
In our study, all of the 31 fetuses had abnormal UA
blood flow. The perinatal morbidity and mortality risk in
14 patients with absent UA end-diastolic blood flow was
28% (4/14) in the retrograde group and 7% (1/14) in the
anterograde group. In five patients with reverse UA end-
diastolic blood flow, perinatal morbidity and mortality
risk was 40% (2/5) and 60% (3/5), respectively. The cause
of such a high mortality rate in the reverse UA end-dia-
stolic flow group may be the gestational age at birth
(<28 weeks) and/or the abnormal (retrograde AI and DV
Doppler indices. Cerebral blood flow has an efficient
auto-regulation mechanism. In the case of increased vas-
cular resistance in peripheral vessels and fetal hypoxemia,
cerebral vasodilatation occurs and a brain-sparing effect
results. Still, an MCA PI less than the 5th percentile due
to the brain-sparing effect is not significantly associated
with increased perinatal morbidity and mortality (7,9).
An absent or reversed “a wave” in the DV or pulsatility
in the umbilical vein is related to abnormal venous blood
flow and the changes have been associated with fetal aci-
dosis at a sensitivity of 70–90% and specificity of 70–80%.
Still, the preterm birth risk for fetuses with growth restric-
tion is 25% with a 65% sensitivity and 95% specificity
(19). Baschat et al. (14,20) found that fetuses with reverse
UA end-diastolic blood flow and abnormal DV blood flow
have higher rate of intrauterine death compared with nor-
mal fetuses. In our study, an absent “a wave” was detected
in 29% (9/31) of patients, and both perinatal morbidity
and mortality were 33.3% (3/9). All the pregnancies with
absent end-diastolic flow in the DV were terminated due
to the fetal or obstetric complications, and we did not
wait for end-diastolic flow to reverse. The fetuses from all
intrauterine death cases were smaller than 28 gestational
weeks, and all had reverse UA blood flow.
Abnormal UA and MCA Doppler flow-related fetal
hypoxia were “early change,” whereas abnormal venous
Doppler flows was determined to be a “late change” when
associated with fetal acidosis. Detection of progression
from hypoxia to acidosis is crucial to decide the optimal
time of delivery to prevent fetal acidosis and fetal demise.
For this reason the AI is thought to be a new horizon for
FGR. The AI is the only vessel that provides blood from
both the right and left ventricular systems.
Fouron et al. (11) reported that neurological develop-
ment in children two to five years of age who had FGR
and abnormal UA blood flow was better for those who
had anterograde AI blood flow rather than retrograde
(11). The most important limitation of this study was the
sample size. To rule out the poor outcomes and to iden-
tify the predictive role of AI blood flow according to ges-
tational age, larger prospective studies are required.
660 Acta Obstetricia et Gynecologica Scandinavica ª 2013 Nordic Federation of Societies of Obstetrics and Gynecology 92 (2013) 656–661
K. Abdelrazzaq et al.
In conclusion, this study suggests that AI Doppler mea-
surements are useful to identify FGR before deterioration
of DV blood flow and into fetal acidosis. These results
support that abnormal AI blood flow increases total peri-
natal morbidity and mortality rates. Although gestational
age is the most important predictor of perinatal compli-
cations, Doppler monitoring helps to detect deterioration
of fetuses with FGR.
Funding
No special funding.
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