© 1988 S.

Kargcr AG, Basel

Fetal Ther 1988;3:31-36 0257-2788/88/0032-003 IS2.75/0

Differential Diagnosis of Small-for-Gestational Age Fetuses by

Doppler Ultrasound1
Domenico Arduini, Giuseppe Rizzo
Department of Obstetrics and Gynecology, Université Cattolica S. Cuore, Rome, Italy

Key Words. Doppler ultrasound • Intrauterine growth retardation • Growth potential •

Differential diagnosis

Abstract. The purpose of this investigation was to compare the efficacy of conventional
ultrasonographic measurements (i.e. head to abdomen circumference ratio, amount of
amniotic fluid) with Doppler ultrasonography in the differential diagnosis of small-for-ges-
tational age (SGA) fetuses. Blood flow velocity waveforms were recorded from the umbilical
artery descending aorta and internal carotid artery in 121 intrauterine growth-retarded
fetuses and the pulsatility index was evaluated as an index of vascular impedance. Conven­
tional ultrasonographic measurements were of limited usefulness in the differential diagno­
sis, whereas the ratio between the pulsatility indexes from umbilical and carotid arteries
proved to be a good index for discriminating SGA fetuses due to low growth potential
(congenital infections, strucutural anomalies, chromosomal abnormalities, constitutional
factors) from those caused by placental dysfunction (specificity 96.6%, sensitivity 89%, pos­
itive predictive value 98.7%, negative predictive value 74.3% and accuracy 90.9%).

Introduction tal pathologies imposed by the supply of nu­

Small-for-gestational age (SGA) fetuses
can be the result of multiple and various eti­
ologies such as low growth potential due to
chromosomal aberrations, congenital infec­
tions and malformations and constitutional
factors, or a variety of maternal and placen­
1 Presented at the International Symposium 'Cur­
trients to the fetus across the placenta [1]. In
clinical practice it is most important to dis­
tinguish the SGA fetuses due to nutrient lim­
itations from those of genetic causes as the
former group is particularly at risk for hyp­
oxia, perinatal mortality and morbidity [2],
Doppler ultrasonography, by providing a
noninvasive assessment of uteroplacental
and fetal circulation, promises to become a
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rent Status of Fetal Medicine and Its Future’, Troina helpful tool in the management of SGA fe­
(Italy), June 12-14, 1988. tuses [3].
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32 Arduini/Rizzo

The aim of this investigation was to com­ percentile according to the nomograms of Campbell
pare the diagnostic value of Doppler ultra­ and Wilkin [4); (3) postnatal confirmation of a birth
weight below the 10th percentile for the Italian popu­
sonography with that of conventional ultra­ lation standard [5], and (4) the presence of exhaustive
sound measurements in the differential diag­ obstetrical and neonatal follow-up.
nosis of SGA fetuses. Fetal blood flow velocity waveforms were re­
corded from the umbilical artery (UA), descending
aorta (DA) and internal carotid artery (1CA) by means
Materials and Methods of commercially available pulsed Doppler equipment
(Ansaldo, Esacord 81). Recordings were performed
121 pregnancies, referred to the Fetal Physiology on patients lying in a semirecumbent position during
Laboratory of our institution for suspected SGA fe­ the period of fetal rest and apnea according to pre­
tuses and fulfilling the following criteria, were en­ viously reported techniques [6].
rolled in this study: (1) singleton pregnancy with reli­ Vascular resistance was evaluated over 10 consec­
able gestational age as assessed by certain last men­ utive cardiac cycles by means of the pulsatility index
strual period and early second trimester ultrasono­ (PI) as described by Gosling and King [7] (PI = [sys­
graphic examination; (2) abdominal circumference tolic velocity-diastolic velocity]/mean velocity). The
(AC) and/or head circumference (HC) below the 5th ratio between the PI of UA and ICA (UA/ICA ratio)
was also evaluated. PI values were considered abnor­
mal when their values lay outside 2 standard devia­
tions (SD) for our normal ranges [8].
Table 1. Characteristics of fetuses with SGA sec­ Each patient underwent the following examina­
ondary to intrinsic causes (low growth potential) tions: (1) AC, HC and femur ultrasonographic mea­
surements, the ratio between HC and AC was also
n % calculated (HC/AC ratio) [9]; (2) evaluation of am-
niotic fluid volume, oligohydramnios was considered
Chromosomal aberrations 3 10 in the absence of any pocket of amniotic fluid measur­
Congenital infections (toxoplasma) 2 6.6 ing more than 1 cm in a vertical axis; (3) accurate
Major malformations 25 83.3 study of fetal anatomy in search of structural abnor­
Renal diseases 10 malities; (4) maternal and if indicated neonatal blood
Central nervous system diseases 5 screening for infections (toxoplasma, rubella, cyto-
Heart diseases 4 megaly and herpes virus), and (5) prenatal or neonatal
Diaphragmatic hernia 2 karyotyping in selected cases.
Multiple abnormalities 4 Fetal distress was considered in the presence of
one of the following findings: abnormal cardiotoco-

Table 2. Incidence of abnormal HC/AC ratio ( < 5th percentile of nomogram of Campbell and Thomps [9])
oligohydramnios and UA/ICA ratio (> 2 SD for our reference range [8]) in the SGA fetuses according to the
étiologie factors

Intrinsic causes No obvious causes X2

(n - 30) (n = 91) P^s

n % n %

Abnormal HC/AC ratio 17 56.6 40 43.9 n.s.

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Oligohydramnios 19 63.3 51 56.0 n.s

Abnormal UA/ICA ratio 1 3.3 81 89.0 0.001
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Doppler and SGA Fetuses 33

grams (i.e. late decelerations, repetitive variable de­ The results of blood flow velocity wave­
celerations): a 5-min Apgar score of less than 7, and form analyses are reported in figures 1-4.
umbilical arterial pH of less than 7.25.
The data were analyzed with the standard diag­
The isolated analysis of PI from UA showed
nostic test parameters: sensitivity; specificity; nega­ an acceptable level of sensitivity in differen­
tive predictive value; positive predictive value, and tiating the two groups of SGA fetuses, but a
accuracy. To compare the different test variables. low specificity. Specificity was improved by
Cohen’s Kappa index was calculated: Kappa values using the PI of DA and ICA, but sensitivity
below 0.2 indicate the absence of agreement; values
between 0.2 and 0.7 fair agreement; values between
0.7 and 1 good agreement, and a value of 1 would
reflect the perfect agreement between the actual con­
dition and the test variable [10]. Differences in fetal
outcome were compared by means of x2 test.

Results

The gestational age at which patients

were referred to our laboratory ranged from
22 to 40 weeks (mean ± SD, 32.4 ± 4.4). 30
cases showed evident fetal causes of SGA as
reported in table 1, whereas no obvious in­
trinsic causes were found in the remaining
fetuses. Table 2 reports the incidence of ab­
normal HC/AC ratio and of oligohydram­
nios in the SGA fetuses grouped according to
the causative factors. No significant differ­
ences were found between the groups consid­
ered.
Fig. 1. Pulsatility index (PI) for the umbilical ar­
tery (UA) of 121 SGA fetuses recorded at the time of
hospital admission, o = SGA secondary to intrinsic
fetal causes (congenital infections, structural anoma­
lies, chromosomal abnormalities); ▲ = SGA without
obvious causes of growth defect (placental dysfunc­
tion, constitutional). Normal ranges for gestation are
shown as mean ± 1 and 2 SD.

Fig. 2. Pulsatility index (PI) for

the descending aorta (DA) of 121
SGA fetuses recorded at the time of
hospital admission. For explana­
tion of the symbols see figure 1.
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Normal ranges for gestation are

shown as mean ± 1 and 2 SD.
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34
significantly decreased. The UA/ICA ratio
was the best index to differentiate the two
groups of SGA fetuses as proven by the high
Cohen’s Kappa index value obtained (ta­
ble 3).
An abnormal UA/ICA ratio was, how­
ever, seen in 1 of the SGA fetuses secondary
to intrinsic causes. This fetus, with retro­
spectively diagnosed bilateral renal agenesis,
developed acute fetal distress 2 days after
Doppler analysis and the placenta showed
multiple infarcts at birth. 10 fetuses without
any evident cause of SGA showed a normal
UA/ICA ratio. Only 1 of these fetuses (10%)
developed fetal distress (i.e. variable deceler­
Arduini/Rizzo
Fig. 3. Pulsatility index (P) for
the internal carotid artery (1CA) of
121 SGA fetuses recorded at the
time of hospital admission. For ex­
planation of the symbols see fig­
ure 1. Normal ranges for gestation
are shown as mean ± 1 and 2 SD.
Fig. 4. UA/ICA ratio of 121
SGA fetuses recorded at the time of
hospital admission. For explana­
tion of the symbols see figure 1.
Normal ranges for gestation are
shown as mean ± 1 and 2 SD.
ations) during late labor. On the other hand,
59 of the 82 (71.9%) fetuses with an abnor­
mal UA/ICA ratio developed fetal distress
and the incidence was statistically higher
when compared to the SGA fetuses with nor­
mal blood flow (x2 p < 0.001).
Discussion
The management of SGA fetuses requires
early identification of the factors which
might impair fetal growth. Conventional ul­
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trasound by means of HC/AC ratio or am-
niotic fluid volume estimation has proved to
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Doppler and SGA Fetuses 35

Table 3. Comparison of standard diagnostic test cerebral vasodilation, and these modifica­
parameters in the differential diagnosis of IUGR tions affect the UA/ICA ratio. Table 4 sum­
fetuses
marizes the hemodynamic features of these
UA DA ICA UA/ICA two groups of fetuses. It must be pointed out
that the isolated assessment of umbilical
Specificity 53.2 92.1 93.6 96.6 waveforms is not always helpful in the differ­
Sensitivity 85.0 59.3 45.2 89.0 ential diagnosis of SGA because oligohy­
Positive pre­
84.2 95.1 95.1 98.7
dramnios [12] or abnormalities in the pla­
dictive value
Negative pre­ cental small vessels [13] may influence um­
dictive value 55.3 43.2 36.8 74.3 bilical resistance alone. Moreover, the asso­
Accuracy 77.2 67.4 58.9 90.9 ciation of a normal UA/ICA ratio and SGA
Kappa index 0.39 0.38 0.25 0.74 should alert to the possibility of fetal congen­
ital abnormalities as clearly demonstrated by
our experience. The absence of these anoma­
lies suggests the existence of a ‘constitution­
Table 4. Vascular resistance in SGA fetuses: al’ cause for SGA, probably due to congeni­
Doppler findings according to etiological factors tal low growth potentiality without increased
Nutrient Low growth risk of perinatal mortality and morbidity.
limitation potential Doppler ultrasonography seems, there­
fore, to be a useful tool in the differential
Uterine arteries N or t N or Î diagnosis between SGA fetuses and can thus
Umbilical artery t N or Î
determine the subsequent obstetric manage­
Descending aorta Î N
Internal carotid artery i N ment. The identification of SGA fetuses sec­
Umbilical/carotid ratio tt N ondary to nutrient limitations might lead to
new therapeutic measures and allow more
N = Normal; t = increase; 1 = decrease. discerning use of antenatal resources. Finally
the feasibility of monitoring the hemody­
namic condition and predicting the occur­
rence of acute fetal distress may influence
be of limited value in differentiating SGA the timing of delivery of these fetuses in the
fetuses. near future.
On the other hand, our results in agree­
ment with the preliminary experience of
Wladimiroff et al. [3], obtained in a limited References
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