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268
WOMEN’S IMAGING
days, and (c) the absence of abnormalities (eg, GA. The MSD is the average of the orthogonal
abnormal bleeding, use of hormonal birth con- diameters of the gestational sac. The MSD lacks
trol) in the cycle immediately preceding concep- the accuracy of CRL measurements; therefore,
tion. If these requirements are met, the due date many societies recommend deferring defini-
is 280 days from the first day of the LMP. Even tive dating until an embryo is visible (12,18). A
when these conditions are met, LMP dating gestational sac without any content represents
introduces error because it assumes that ovula- a probable intrauterine pregnancy (IUP); a sac
tion invariably occurs on day 14 of a 28-day with a yolk sac or embryo, a definite IUP; and a
cycle (12). In addition, up to 50% of women sac with an embryo smaller than 7 mm without
do not know their LMP, and nearly half of all cardiac activity, a pregnancy of uncertain viability
pregnancies in the U.S. are unplanned (13). (19). For probable and definite IUP without an
In one randomized trial of US-based dating, embryo, follow-up US is recommended to deter-
40% of women randomly assigned to undergo mine viability and definitively establish pregnancy
first-trimester US had altered dates owing to a dates (Fig 1) (20). Once an embryo is visible, the
discrepancy of greater than 5 days (14). When CRL is measured, and it alone (not a composite
the LMP is unknown or does not fit the param- of CRL and MSD) is used to estimate the GA
eters noted above, first-trimester US should be (Fig 2) (12,21). In cases of spontaneous twins (or
used to corroborate or establish the gestational other multifetal gestations), the CRL of the larg-
date (12). est embryo or fetus should be used to establish
dates in the first trimester (before 14 0/7 weeks
Sonographic Dating in the First Trimester [14 weeks, 0 of 7 days]) (22).
Several studies (12,15–17) have demonstrated In addition to during scheduled first-trimester
that first-trimester measurement of the crown- dating US, sonologists can encounter pregnan-
rump length (CRL) is highly accurate for preg- cies in other settings such as in the evaluation of
nancy dating. In the first trimester, growth is most pelvic pain and bleeding. Emergency department
dependent on underlying embryologic events. visits can precede the first prenatal visit, and
As the fetus enters the second and especially clinical or other pregnancy dates may not yet be
the third trimesters of pregnancy, constitutional established. At US scanning in these settings, the
factors begin to influence the fetal growth trajec- LMP and any size-date discrepancy should be
tory (12). Simply stated, a fetus whose DNA is documented to establish or corroborate preg-
derived from parents of smaller stature will, by nancy dates as early as possible.
virtue of its genetic makeup, be smaller compared
with the average population of fetuses of the same Sonographic Dating in the Second
GA. A similar corollary exists for larger fetuses. In Trimester
contrast, fetuses whose growth is compromised by At 14 0/7 weeks (CRL, ?84 mm), the accuracy of
aneuploidy, placental insufficiency, or overgrowth the CRL for dating begins to decline owing to the
syndromes demonstrate a growth pattern that is technical challenges of visualizing the full length of
not concordant with their anticipated or consti- the fetus and the increased possibility of measure-
tutional growth potential. Their abnormal size ment error due to fetal positioning (17). Given the
reflects the underlying anomaly. increasing inaccuracy of US dating with advanc-
Because constitutional and pathologic factors ing GA, a pregnancy in which US confirmation
affect early embryonic growth the least, the ac- or GA revision occurs after 22 0/7 weeks should
curacy of US for gestational dating is highest in be considered suboptimally dated (12). Recom-
early pregnancy and diminishes with advancing mendations for adjusting gestational dating that
GA. Therefore, the dates established with first- take into consideration the standard deviation of
trimester US should not be altered by future US biometric parameters at varying GAs can be found
examinations. However, review of the original in American College of Obstetricians and Gyne-
images is preferable, whenever possible, for evalu- cologists Committee Opinion No 700: Methods
ating the measurement technique and ensuring for Estimating the Due Date (12). It is important
accuracy. Commonly used US-based pregnancy to acknowledge that not all pregnant women pres-
dating criteria suggest that a discrepancy of ent for care in the first trimester. For these women,
greater than 5 days between the LMP- and US- many of whom have increased risk factors for poor
derived dates is sufficient to change the EDD obstetric outcomes, a systematic approach to cor-
early in the first trimester. However, by 28 weeks, roborating or modifying the gestational dating at
a discrepancy of greater than 21 days is required later points in the pregnancy has the potential to
for this change (12). improve perinatal outcomes.
Before the emergence of a visible embryo, the In the second trimester, GA assessment is
mean sac diameter (MSD) is used to estimate the based on standard biometric measurements of
RG • Volume 41 Number 1 Debbink et al 271
Figure 1. Early first-trimester measurements and milestones. (a) US scan shows the MSD, which is the aver-
age of orthogonal diameters of the gestational sac measured from inner border to inner border. The MSD can
be used to calculate the GA before an embryo is visible. An intrauterine sac–like structure without a yolk sac or
embryo, as seen in this example, is described as a probable intrauterine pregnancy. Follow-up US is performed
at 14 days, at which time a live embryo should be visible. (b) US scan shows an intrauterine sac–like structure
with a yolk sac or embryo—that is, a definite intrauterine pregnancy. Follow-up US for assessment of a sac with
only a yolk sac is performed at 11 days, at which time a live embryo should be visible. If an embryo with a CRL of
less than 7 mm without cardiac activity is present, follow-up US is performed at approximately 7 days to ensure
viability. Transvaginal US is preferred for accurate measurement.
head circumference, biparietal diameter (BPD), particularly useful in those pregnancy cases in
abdominal circumference (AC), and femoral which growth abnormalities are suspected but the
diaphysis length (Figs 3–5) (18). In cases of gestational dates are nonverified (Table 1) (28). Of
multifetal gestation, the fetus with the larger head note, TCD, renal length, and foot length nomo-
circumference should be used to establish the grams are available at the open access website
GA after 14 0/7 weeks (22). A number of for- www.perinatology.com. Other sonographic markers
mulas based on these standard parameters exist such as epiphyseal ossification and fetal subcuta-
to estimate fetal weight and GA (23). Standard neous tissue measurement also may corroborate
biometric measurements generally correlate the GA. An important caveat is that adjunctive
well with clinical gestational dates and often are measures should be used only when the feature of
sufficient to confirm or adjust dating in many interest is anatomically or structurally normal.
pregnancies. However, various circumstances can The TCD is easily measured in the axial
make standard fetal biometry less reliable. For oblique posterior fossa view that is used routinely
instance, if a fetus has abnormalities such as ven- during the anatomic survey (Fig 6). In euploid
triculomegaly or ascites, or if the mother presents fetuses with a structurally normal cerebellum, the
late in pregnancy, standard biometry may yield TCD has a log-linear correlation with GA and
a significantly overestimated or underestimated does not change with head shape. It is important
GA. In addition, if fetal growth abnormalities are to note that the GA-TCD correlation appears to
suspected, additional anatomic parameters that be largely preserved in the settings of FGR and
corroborate the menstrual age are useful. macrosomia (29,30). This finding is supported by
human and nonhuman primate studies (31,32)
Adjuncts to Standard Biometry that demonstrate the preservation of cerebellar
Several fetal anatomic structures demonstrate blood flow in fetuses with growth restriction.
consistent growth throughout the latter half of ges- Fetal foot length is a commonly used sono-
tation, and measurements of these structures reli- graphic and postnatal anatomic correlate to GA
ably correlate with GA. Of these measurements, (Fig 7) (25,33). Although the fetal foot length is
transcerebellar diameter (TCD), foot length, not exempt from the effects of global FGR, this
renal length, and sacral length are among those measurement is particularly useful in the setting of
for which there are published validated nomo- other anomalies, such as anencephaly, ascites, and
grams (24–27). In some instances, these structures shortened long bones (eg, in skeletal dysplasia).
maintain their relationship with GA even when Renal size is another anatomic measure-
growth abnormalities are present, making them ment that provides corroboration for gestational
272 January-February 2021 radiographics.rsna.org
dating. In the absence of renal anomalies or to perform than the other described measure-
rare overgrowth syndromes such as Beckwith- ments but is an important adjunct to standard
Wiedemann syndrome, renal dimensions correlate biometry (Fig 9).
well with GA (26,34). Renal length is measured Ossification of the long bone epiphyses occurs
in a longitudinal plane in the cephalocaudal in the third trimester. The staggered appearance
direction and has a linear relationship with GA of ossification centers provides insight into the
(Fig 8). Although the renal volume diminishes likely ranges of GA. This is particularly useful in
with FGR, the renal length remains relatively the setting of advanced gestation, when biometry
constant (34,35). Because of this constant is unreliable, and in cases of possible macrosomia
relationship with GA, renal length, like TCD, or FGR, when there is concern for inaccurate
can provide important adjunctive information dating (28). The DFE, PTE, and PHE have been
regarding the GA, even in the setting of growth studied most closely, with early work showing a
abnormalities. Renal length is easily measured close correlation between the appearance of os-
in the third trimester, representing an important sification centers and the fetal lung maturity, as
additional measurement at a point in pregnancy demonstrated at amniocentesis (38).
when the accuracy of standard fetal biometry More recently, the appearance and even the
decreases. measurement of the epiphyses have been cor-
Sacral length also correlates linearly with related with GA. The DFE ossification center
gestational dates and appears to have a stable appears as a hyperechoic stippled or solid ovoid
relationship with GA, even in the setting of structure within the hypoechoic cartilaginous
growth abnormalities (27,36,37). This measure- epiphysis of the distal femur at 32–33 weeks ges-
ment is somewhat more technically challenging tation (Fig 10). This ossification center is present
RG • Volume 41 Number 1 Debbink et al 273
Figure 5. Femur length. US scan shows the femur Figure 6. TCD measurement. On a standard trans
length (FL)—that is, the length of the femoral diaphy- cerebellar (or posterior fossa view) US scan, the TCD
sis—measured on the long axis of the femur, perpen- is measured across the widest point of the cerebellum,
dicular to the insonating beam. It is measured from end with calipers (*) placed on the lateral outer edges.
to end, excluding the distal epiphyses (E).
positive predictive value for determining a GA of been associated with poor perinatal outcome and
greater than 37 weeks (40). is predictive of pathologic FGR. Wu et al (43)
Finally, fetal subcutaneous tissue measure- suggest that lower abdominal wall thickness may
ments may prove useful for validating the GA, correlate with the lack of metabolic reserve that
assessing fetal metabolic reserve, and predicting characterizes pathologic FGR. Others have pro-
the neonatal outcome of fetuses with growth posed the use of abdominal wall thickness in the
abnormalities (Fig 13) (41–43). Published nomo- evaluation of macrosomia (44,45). In one study
grams show that lateral abdominal wall thickness involving women with pregestational diabetes, an
increases linearly, approximately 0.19 mm per abdominal wall thickness greater than 6.35 mm
week, with gestation (41). In the third trimes- at 34 weeks gestation accurately predicted birth
ter, low abdominal subcutaneous thickness has weight greater than the 90th percentile (46).
RG • Volume 41 Number 1 Debbink et al 275
Figure 10. DFE measurement. (a) US scan shows femur length measurement in a fetus at 24 weeks
gestation, with the epiphysis (E) seen as a homogeneous hypoechoic structure without internal calcifica-
tion. (b) US scan shows femur length measurement in the same fetus at 34 weeks, with the epiphyseal
ossification center (arrow) seen as a central echogenic focus within the epiphysis. The DFE is usually visible
after 32 weeks gestation. (c) Coronal US image through the knee shows a potential pitfall in the assess-
ment of DFE ossification. The echogenic region (arrow) is created by synovial folds in the intercondylar
notch. The DFE and PTE are well seen, and neither is ossified.
Figure 11. PTE in two fetuses. (a) Coronal US scan through the knee of a 30-week-old fetus shows the
unossified PTE (arrows) as a homogeneous hypoechoic structure without internal calcification. (b) Coro-
nal US scan through the knee of a 36-week-old fetus shows the epiphyseal ossification center (arrow) as a
central echogenic focus within the epiphysis. The PTE is usually visible after 35 weeks gestation.
definitions and labels for inappropriate fetal size ary 2018 issue of American Journal of Obstetrics and
(Table 2) (47). The lack of consensus is due in Gynecology (48), which is focused on fetal growth
part to varying standards for assessing fetal size, as standards.
well as varying capability of percentile thresholds It is also important to note that each US soft-
for accurate identification of those fetuses at risk ware manufacturer chooses a fetal growth formula
for complications. Although a full review of fetal for its reporting package; therefore, formulas for
growth standards is beyond the scope of this work, determining fetal weight percentages vary across
it is worth noting that numerous fetal growth platforms. It would behoove sonologists to become
curves exist, have proliferated rapidly in the past familiar with the formula used for their reporting
decade, and enable the identification of fetuses package and the associated limitations.
at risk for complications with varying degrees of To briefly review, early fetal growth standards
success (23,48). Interested readers may find an (eg, those of Brenner and Williams) were derived on
additional relevant discussion in the special Febru- the basis of birth weights of both live and stillborn
RG • Volume 41 Number 1 Debbink et al 277
Figure 12. PHE in two fetuses. (a) Coronal US scan through the shoulder of a 33-week-old fetus shows the
unossified PHE as a homogeneous hypoechoic structure (arrow) without internal calcification. (b) Coronal US
scan through the shoulder of a 41-week-old fetus shows the epiphyseal ossification center (arrow) as a central
echogenic focus within the epiphysis. The PHE is usually visible after 38 weeks gestation.
Figure 13. Lateral abdominal wall fat thickness. (a) US scan shows lateral abdominal wall thickness,
which is measured in the same plane as the AC, perpendicular to the ultrasound beam, excluding the rib
and any hypoechoic muscle, at the thickest area in the near field. In this example, the abdominal wall
fat thickness is 5.3 mm at 37 weeks, between the 75th and 95th percentiles. Fat thickness of less than 3
mm at 36 weeks gestation predicts growth restriction and low birth weight, whereas increased abdomi-
nal wall fat thickness is associated with an increased rate of cesarean section, especially in the setting of
maternal diabetes. PV = portal vein for orientation on this magnified image of the fetal abdominal wall at
the level of the AC. (b) US scan shows fetal macrosomia, which tends to be associated with fat accumu-
lation in other body areas (eg, thigh, cheek, upper thorax), as shown in this fetus of a diabetic mother,
with marked subcutaneous fat deposition in the chest wall (arrows). The infant was macrosomic at birth.
(c) For comparison, a case of fetal hydrops with skin edema is shown. Transabdominal US scan axial to
the fetal abdomen shows skin edema (x to x), which is hypoechoic, unlike subcutaneous fat, which is
echogenic. (d) Transabdominal US scan axial to the fetal chest at the level of four-chamber heart view
in the fetus in c confirms the presence of hypoechoic skin edema (arrows) and shows pleural effusion.
278 January-February 2021 radiographics.rsna.org
Figure 14. EFW trajectory in a sonographically redated third-trimester pregnancy. Chart (a)
and graph (b) show fetal measurements (a) and appropriate interval growth (b) after sono-
graphic redating to 33 weeks gestation in a patient who had limited prenatal care and was
referred owing to suspected FGR. At presentation, her gestational dates were off by 23 days,
ossification was present in the DFE only, and the renal and cerebellar sizes suggested a GA of
33 weeks. Amniotic fluid volume and cord Doppler US findings were normal, and the fetus was
active. The LMP-based GA was changed to a US-based GA, and a 3-week follow-up study con-
firmed appropriate interval growth (b). Data on the horizontal axis in b are GAs. The patient
delivered a healthy infant at term. Correct dating avoided induction of labor and iatrogenic
preterm delivery resulting from an incorrect diagnosis of growth restriction. FL = fetal length,
FW = fetal weight (vertical axis in b), HC = head circumference.
infants of varying GAs (49,50). One limitation of downward. Consequently, using these standards
growth curves developed according to birth weights to assess all ongoing pregnancies will result in
is that the weights of infants born at early GAs fewer fetuses being assigned to a low–fetal-weight
often are, on average, lower than the weights of percentile (eg, <10th percentile). Some argue that
fetuses in ongoing pregnancies. In other words, the these curves may fail to include some pathologi-
population of fetuses delivered at 29 weeks owing to cally small fetuses. Other growth standards (eg,
a combination of stillbirth, maternal complications Hadlock, INTERGROWTH-21, World Health
(such as preeclampsia with severe features), and Organization) are based on US measurements
obstetric complications (such as chronic abruption of presumably healthy fetuses of various GAs
or bleeding previa) includes many more fetuses (51–53). In addition, more recent standards based
with impaired growth than does the population of on large amounts of data may provide customized
fetuses in ongoing pregnancies at 29 weeks. curves that account for maternal weight, age, race,
The higher proportion of smaller fetuses in the and fetal sex (54). However, it appears that the
delivered population shifts the mean fetal weight performance of these curves in identifying fetuses
RG • Volume 41 Number 1 Debbink et al 279
at risk for complications may not surpass that of refine the determination of which fetuses are
the noncustomized Hadlock curve (48). most at risk for adverse perinatal consequences.
patient whose menstrual dating was verified at US identified, genetic information may be obtained by
in the first trimester than it is in a maternal patient using noninvasive screening tests such as cell-free
who received late care and has uncertain dates. fetal DNA testing, or, preferably, diagnostic amnio-
In the latter setting, use of some of the nonstan- centesis. Viral studies of the amniotic fluid also may
dard biometric parameters and assessment of be performed if clinically indicated.
epiphyseal ossification centers may help to narrow Maternal infections, including TORCH (toxo-
the range of possible GAs. Careful attention to plasmosis, other infections [parvovirus, syphilis,
stigmata of overgrowth syndromes is important, as human immunodeficiency virus, etc], rubella,
these may preclude the use of some biometric ad- cytomegalovirus, and herpes), also can contribute
juncts. For instance, syndromic renal enlargement to FGR. Of these, cytomegalovirus is the most
in Beckwith-Wiedemann syndrome precludes the common (58,61). In addition to maternal clinical
use of renal length for GA corroboration. symptoms, US findings may include calcifications
in the brain, abdominal organs, and placenta;
Managing Pregnancies Affected by hepatosplenomegaly; and brain lesions such as
Abnormal Fetal Growth parenchymal cysts, ventriculomegaly, and cerebral
migrational disorders. Maternal serum testing with
FGR: Initial Diagnosis immunoglobulin G and immunoglobulin M titers
Typically, FGR is diagnosed no earlier than the may help to establish the chronicity of maternal
middle of the second trimester, around the time of cytomegalovirus infection. Positive immunoglobu-
the fetal anatomic survey. An EFW lower than the lin G and immunoglobulin M levels with low im-
10th percentile for GA should prompt additional munoglobulin G avidity are concerning for acute
investigation, and ascertaining the accuracy of the cytomegalovirus infection (66). A review of the
gestational dating is first and foremost in this pro- indications for and interpretation of maternal test-
cess. Subsequently, a detailed sonographic assess- ing for infection is beyond the scope of this article.
ment aids in the difficult task of separating fetuses However, interested readers can refer to the spe-
with an EFW lower than the 10th percentile into cial May 2006 issue of Reproductive Toxicology (66).
those who are physiologically small but healthy A review by Crino and Driggers (67) provides an
and those who are pathologically growth restricted overview of specific sonographic findings that raise
and therefore at risk for perinatal morbidity and suspicion for certain viral infections.
mortality. Placental insufficiency tends to result in
The assessment should focus on sonographic FGR in the third trimester, but severe cases can
findings that are consistent with the three main manifest earlier (61,68). US findings are less
causative diseases in FGR: aneuploidy, infection, specific but can include diminished amniotic
and placental insufficiency. Aneuploidy tends to fluid volume and decreased placental volume
cause FGR early in gestation and may account with increased placental echogenicity or calcifi-
for as many as 20% of cases of FGR diagnosed cation. Placental insufficiency frequently results
before 26 weeks; triploidy and trisomy 18 are the in brain-sparing growth restriction, in which the
most common diagnoses (58,61,65). Triploidy is AC and EFW lag while the head size measured
suspected when there is a significant discrepancy by using the BPD and head circumference re-
between the head size and body size, with body size mains normal (69). Placental insufficiency may
lagging considerably. Careful attention to anatomic also correlate with maternal disease, most com-
structures and relative biometric features is crucial monly antiphospholipid antibody syndrome and
for identifying constellations of findings associ- preeclampsia with severe features (70). Maternal
ated with common aneuploidies and syndromes. well-being should be closely tracked, especially
Assessment of amniotic fluid volume is an integral when severe FGR is identified.
part of evaluation. The amniotic fluid volume is The timing of the diagnosis of FGR may
typically quantified by measuring the maximal provide clues to the cause. Previously, the terms
vertical pocket (MVP) before 28 weeks gestation. asymmetric fetal growth restriction and symmetric
The amniotic fluid index—that is, the sum of the fetal growth restriction were used to describe osten-
four deepest pockets free of fetal parts or umbilical sibly distinct causes, but these have largely been
cord—is measured after 28 weeks, when a larger abandoned in favor of early- and late-onset FGR,
fetal size allows reproducible four-quadrant mea- with most authors defining late-onset growth
surements. MVP depths are used to define oligo- restriction as growth restriction diagnosed after
hydramnios (MVP <2 cm) and polyhydramnios 32 weeks gestation (Table 3) (71–73).
(MVP >8 cm) throughout the second and third
trimesters. The amniotic fluid volume is frequently FGR: Follow-up and Surveillance
normal with aneuploidy, but it is reduced in the During pregnancies complicated by FGR, surveil-
setting of placental insufficiency. When FGR is lance is warranted to allow intervention that may
RG • Volume 41 Number 1 Debbink et al 281
prevent or reduce morbidity and mortality. Thus, decreasing from 10th to 5th percentile to less
surveillance should begin only when the fetus than 1st percentile) should be cause for alarm
reaches a size and GA at which intervention is likely (Fig 15). On the other hand, fetuses with sus-
to be successful. Neonatal resuscitation success pected growth restriction who are constitutionally
and limitations vary among hospitals. Although the small tend to follow their growth curve over time
lower limits of resuscitation have decreased across without crossing percentiles (Fig 16).
the United States, few institutions routinely offer
neonatal resuscitation at less than 23 0/7 weeks FGR: Doppler US Studies for Risk
gestation. Neonatal survival, neurologically intact Stratification
survival in particular, is still relatively rare for neo- The application of Doppler waveforms to identify
nates in the 23rd gestational week or who weigh less high-risk FGR has evolved considerably from its
than 500 g (74). Ideally, discussions regarding life- earliest use. Doppler indices and ratios involving
saving interventions in the setting of severe FGR multiple fetal and maternal vessels have been as-
should occur in a patient-centered multidisciplinary sessed for their utility in the management of FGR.
fashion, with input from maternal-fetal medicine However, the usefulness of these measurements in
and neonatology colleagues. predicting perinatal morbidity and mortality in the
Mothers whose fetuses have an EFW lower setting of FGR beyond that of standard umbilical
than the 10th percentile for GA should undergo artery (UA) Doppler US is limited (58).
serial growth US in 3–4-week intervals after
the diagnosis. Owing to the margin of error in UA Doppler US.—UA Doppler US provides a
sonographic biometry, the EFW should not be window into the health of the fetoplacental unit.
routinely measured more frequently than every The fetoplacental circuit is normally a low-resis-
3 weeks (18,75). Serial measurements provide a tance system in which the fetus obtains nutrients
growth trajectory, allowing the managing clini- and eliminates metabolic waste with little cardiac
cian to continuously reevaluate viability, perinatal effort. Under normal circumstances, blood flow
risk, and delivery timing. Although investiga- from the fetal descending aorta into the UAs and
tors in several studies have attempted to identify toward the placenta should occur during both sys-
trajectory models that might aid in identifying tole and diastole, a testament to the low resistance
at-risk fetuses, as yet the data are insufficient in the placental bed (Fig 17) (59). Placental insuf-
to promote statistical trajectory modeling as a ficiency represents the clinical end point of various
clinical tool (76). That said, fetal growth that has mechanisms that alter placental vascular compli-
halted or fallen across multiple percentiles (eg, ance by way of changes in the small muscular
282 January-February 2021 radiographics.rsna.org
Figure 17. UA Doppler waveforms. Top row: Normal low-resistance flow in the UA in the third trimester, with continuous an-
tegrade diastolic flow and a systolic-diastolic ratio of 2.86. Second row from top: Elevated UA resistance, with increased placental
resistance manifesting as decreased diastolic flow and an abnormal systolic-diastolic ratio (6.76). Third row from top: Absence of
end-diastolic flow, which is always abnormal. Bottom row: Decrease in UA flow to below the baseline at diastole, indicating reversed
end-diastolic flow, which is an ominous finding. The cited delivery date goals are those recommended in the clinical guidelines of
the Society for Maternal-Fetal Medicine (59) and should be interpreted in the full clinical context, including other maternal or fetal
findings that may dictate delivery earlier than the stated GA.
prematurity. Thus, UA Doppler US is generally societies in the United States caution that there
not performed until there is a reasonable expec- are insufficient data supporting improved out-
tation of successful neonatal resuscitative efforts comes to recommend the routine clinical use of
(usually at >23 weeks gestation). ductus venosus Doppler US (59).
In rare circumstances, such as previable severe
FGR with a suspected placental cause, reversed Middle Cerebral Artery Doppler US.—Fetal
or absent end-diastolic flow may corroborate the hypoxia results in preferential redistribution of
placental cause of the disease and predict im- oxygenated blood toward the brain, the so-called
pending fetal death. This information may help to brain-sparing effect (69). Middle cerebral artery
appropriately prepare the maternal patient for a (MCA) Doppler US can be easily performed,
poor obstetric outcome; however, it should not be and under normal circumstances, the MCA
used as a definitive diagnostic tool. shows a higher resistance waveform than does the
UA, which should have a lower systolic-diastolic
Ductus Venosus Doppler US.—The ductus veno- ratio or pulsatility index than the MCA at all
sus is the first of three physiologic shunts in the times during pregnancy (69,79).
fetal circulation that preferentially guide oxygen- The clinical use of MCA systolic-diastolic
ated blood toward the fetal brain and heart. In ratios or pulsatility indexes for assessment of
the setting of a normal physiologic profile, the FGR is controversial. The cerebroplacental ratio
fetal venous circulation demonstrates persistent (CPR), the ratio between cerebral blood flow (as
forward flow. Increased placental vascular resis- measured with MCA Doppler US) and placental
tance can lead to poor cardiac contractility; when blood flow (as measured with UA Doppler US),
this occurs, forward flow in the ductus venosus is also has been proposed as a measure of fetal well-
impeded and the waveform becomes abnormal. being in the setting of FGR. In a meta-analysis
The clinical use of ductus venosus Doppler (69), the CPR, as compared with standard UA
US is controversial, as it has not been shown to Doppler US measurement, demonstrated supe-
routinely improve perinatal outcomes. Obstetric rior value for the prediction of composite neonatal
284 January-February 2021 radiographics.rsna.org
morbidity and risk of emergency cesarean section FGR: Special Case in Twin Gestations
but no benefit for the prediction of perinatal Fetal growth abnormalities also occur in cases
mortality or other assessed outcomes. MCA of multiple gestations. When only one twin fails
Doppler US alone did not perform better than to fulfill its growth potential, this is referred to
UA Doppler US in the prediction of any assessed as selective FGR (Fig 18). This is of particular
outcomes. Therefore, obstetric societies in the concern in monochorionic pregnancies because
United States caution that the additional infor- the demise of the growth-restricted twin has
mation obtained from MCA Doppler US and potentially catastrophic consequences for the
CPR measurements is insufficient to recommend normally growing twin owing to complex vascu-
their routine use for guiding clinical care (59). lar anastomoses in the shared placenta (81). As
with singleton pregnancies, with twin pregnan-
FGR: Clinical Assessments and cies, inconsistent nomenclature has impeded the
Interventions to Optimize Delivery development of evidence-based management
Timing and Outcome protocols for selective FGR. To address this issue,
Sonographic evaluation of the growth-restricted an international panel of experts used a Delphi
fetus provides crucial information for guiding process to reach a consensus on the definition of
additional clinical assessments. Foremost among selective FGR, as described in Table 4 (82).
these assessments are the nonstress test and UA Doppler US findings in the smaller twin in
modified biophysical profile, which is a combi- a monochorionic pair are used to determine the
nation of the nonstress test and amniotic fluid severity of the selective FGR phenotype (83). With
volume assessment. In cases of suspected placen- type I selective FGR, there is persistent end-dia-
tal insufficiency, a reassuring nonstress test has a stolic flow in the UA. With type II selective FGR,
95% negative predictive value for stillbirth in the there is persistently absent or reversed end-dia-
subsequent week. There is no consensus on the stolic flow. With type III, end-diastolic flow cycles
frequencies at which to perform nonstress tests range between present (even if abnormal) end-
and modified biophysical profiles, and manage- diastolic flow and intermittently absent or reversed
ment varies by institution and perceived severity flow. A type III pattern is also called cyclical flow.
of growth restriction phenotype. Prognoses vary by selective FGR subtype, with the
In preterm fetuses with severe growth restric- worst outcomes occurring in cases of type II gesta-
tion and UA Doppler US abnormalities, daily tion with absent or reversed end-diastolic flow in
or even continuous electronic fetal heart rate the growth-restricted twin. However, cyclical type
monitoring may be recommended as a means of III flow indicates large intertwin vascular connec-
prolonging the pregnancy for as long as possible. tions, creating an unstable situation in which the
In fetuses with a less severe phenotype and/or demise of one twin can occur with little warning.
normal UA Doppler results, less frequent testing Type I selective FGR can be managed expectantly,
may be indicated. At many institutions, nonstress but there is a potential role for fetal intervention in
testing is performed once or twice weekly to type II and type III cases (84).
coincide with the frequency of UA Doppler US
assessments; testing and US frequency are then Fetal Macrosomia and Large for GA:
adjusted according to the findings (58,59). Initial Diagnosis
Other routine obstetric interventions aimed Fetuses that are large for their GA can be identi-
at reducing risks associated with prematurity fied in a number of ways. Typically, the diagnosis
should be performed in the setting of FGR when is made in the third trimester during routine
preterm delivery is anticipated. Before 34 weeks evaluation for maternal risk factors (eg, diabetes)
gestation, antenatal corticosteroids are adminis- or when the clinical measurement of the sym-
tered, ideally 48 hours before delivery, to improve physis-fundal height is abnormal (Fig 19). More
lung maturity and reduce respiratory and other rarely, syndromic overgrowth may be diagnosed
perinatal morbidities. In addition, at between 34 at the time of the fetal anatomic survey.
0/7 and 36 6/7 weeks gestation, if delivery within It is worth noting that the accuracy of US for
the next 7 days is anticipated and steroids have correct prediction of macrosomia is suboptimal.
not been administered previously, a course of an- The suboptimal prediction performance is related
tenatal steroids should be considered. However, to the later GA at which large-for-GA fetuses are
if the fetal status warrants immediate delivery at diagnosed and the poorer performance of EFW
or after 34 weeks gestation, the delivery should formulas at the upper extremes of weight. Meta-
not be delayed in order to administer antenatal analyses (64) demonstrate that US has 56% sen-
corticosteroids. Magnesium sulfate is given be- sitivity and 93% specificity for predicting neonatal
fore 32 weeks gestation for fetal neural protection birth weight greater than 4000 g and decreases in
(58,59,80). accuracy with increasing weight. Only 33%–44%
RG • Volume 41 Number 1 Debbink et al 285
Pregnancy Type EFW Percentile ∆EFW AC Percentile UA-PI Percentile No. of Criteria Needed
MC <10th ≥25% <10th >95th Three of four
DC <10th ≥25% … >95th Two of three
Source.—Reference 82.
Note.—An EFW lower than the 3rd percentile in one twin is sufficient to diagnose selective FGR.
Otherwise, the listed criteria are used in combination. DC = dichorionic, ∆EFW = difference in
EFW between the twins, MC = monochorionic, UA-PI = UA pulsatility index.
Conclusion
Fetal growth abnormalities have a profound ef-
fect on pregnancy management, delivery tim-
ing, and perinatal outcome for the mother and
infant. Fetal size is assessed in relation to what
is expected at any given GA. Therefore, correct
pregnancy dating is critical for the detection and Figure 19. EFW trajectory demonstrating increased
surveillance of abnormal fetal growth and the risk for macrosomia. Graph shows a progressive increase
prevention of perinatal maternal and fetal mor- in the EFW (vertical axis) with advancing GA (horizon-
tal axis). The EFW was greater than the 90th percentile
bidity and mortality. at 32 and 36 weeks GA, whereas earlier US results (at
15 and 21 weeks) were concordant with menstrua-
Disclosures of Conflicts of Interest.—M.P.D. Activities related tion dates. The infant was not actually macrosomic at
to the present article: disclosed no relevant relationships. Activi- birth, weighing 3829 g, but delivery was complicated
ties not related to the present article: grant support from Society by shoulder dystocia and the infant spent several days
for Maternal Fetal Medicine and AMAG Pharmaceuticals to in the neonatal intensive care unit owing to episodes of
investigate severe maternal morbidity in Utah, and from the hypoglycemia. He also had extensive bruising of the left
Larry H. Miller Family Foundation for research and clinical
shoulder and torso.
project on group prenatal care for women with diabetes in
pregnancy. Other activities: disclosed no relevant relationships.
P.J.W. Activities related to the present article: disclosed no rele-
vant relationships. Activities not related to the present article: book 5. Henriksen T. The macrosomic fetus: a challenge in cur-
royalties from Elsevier. Other activities: disclosed no relevant rent obstetrics. Acta Obstet Gynecol Scand 2008;87(2):
relationships. A.M.K. Activities related to the present article: dis- 134–145.
closed no relevant relationships. Activities not related to the pres- 6. Bamberg C, Hinkson L, Henrich W. Prenatal detection
ent article: speaker honorarium from World Class CME, book and consequences of fetal macrosomia. Fetal Diagn Ther
royalties from Elsevier. Other activities: disclosed no relevant 2013;33(3):143–148.
relationships. 7. Gu S, An X, Fang L, et al. Risk factors and long-term health
consequences of macrosomia: a prospective study in Jiangsu
Province, China. J Biomed Res 2012;26(4):235–240.
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TM
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