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The Journal of Maternal-Fetal & Neonatal Medicine
ISSN: 1476-7058 (Print) 1476-4954 (Online) Journal homepage:
Second trimester growth velocities: assessment of
fetal growth potential in SGA singletons
Russell L. Deter, Wesley Lee, John Kingdom & Roberto Romero
To cite this article: Russell L. Deter, Wesley Lee, John Kingdom & Roberto Romero (2017):
Second trimester growth velocities: assessment of fetal growth potential in SGA singletons, The
Journal of Maternal-Fetal & Neonatal Medicine, DOI: 10.1080/14767058.2017.1395849
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Accepted author version posted online: 23
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In the study of fetal growth and growth abnormalities, both size (1-7) and velocity
[change in size over time] (8-16) have been utilized. Although use of size is more
common, growth velocity is a more logical definition of ‘growth’ (14,17).
Working with growth velocities, however, requires serial measurements, definition
of an appropriate interval between scans and a means for acquiring velocity data
over a substantial range of fetal ages (11-16). As a result, only a limited number of
studies have been carried out except for those based on Individualized Growth
Assessment [IGA] (8-10, 18-22), which utilizes comparisons of expected and
measured third trimester average growth velocities (8).
Although most studies of fetal growth velocity have focused on its use in detecting
growth abnormalities, IGA utilizes this parameter primarily as a measure of growth
potential [see Appendix (9)]. Measurements of 2nd trimester growth velocities are
used to specify Rossavik size models which then generate expected 3rd trimester
size trajectories and provide predicted birth characteristics (9). Good agreement
between actual and expected measurement has been obtained in fetus/neonates
with normal neonatal growth outcomes, as measured by Percent Deviations
[%Dev] prenatally (9) and Growth Potential Realization Index [GPRI] values in
the neonate (18). Both %Dev’s and GPRI’s have been shown to be proportional to
the difference between the actual and expected growth velocities in the third
trimester (8).
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Because of easily met fetal nutritional requirements due to small size and the
minimal variability in individual fetal growth during the 2nd trimester [see
Appendix], growth velocity measurements during this trimester has been proposed
to be a manifestation of genetic and other constituent growth controllers (9,23).
These characteristics and others led us to consider the 2nd trimester growth velocity
as an observable variable which can give estimates of the latent variable, Fetal
Growth Potential [Appendix]. This concept of course implies that each anatomical
parameter has its own growth potential and only some composite of growth
velocities (currently undefined) could represent the growth potential of the fetus as
a whole. The justification for considering 2nd trimester growth velocities to be
optimal estimates of fetal growth potential is more thoroughly described in more
detail in the Appendix.
Second trimester growth velocities have been studied extensively in 119 fetuses
The sample, methods and analytical techniques used in this study have been
described previously (10). Only those details pertinent to the current investigation
will be summarized here.
This investigation was carried out using a sample of SGA neonates [birth weight
<10th percentile] obtained retrospectively from three centers: [Perinatology
Research Branch, Detroit, MI [97 cases]; University of Toronto, Toronto, ON [20
cases], Canada; Baylor College of Medicine, Houston, TX [9 cases] (10). Data
were from high risk pregnancies in patients seen in the Center for Advanced
Obstetrical Care and Research [PRB], the Placenta Clinic [Toronto] and the
Maternal Fetal Medicine Ultrasound Clinic [Baylor] under approved protocols
OH97-CH-N067{PRB}, REB Number: 13-0266-C{Toronto}, IRB Number:
H-35518{Baylor)}]. Scans were either part of a research protocol or clinically
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with normal neonatal growth outcomes (9). In only one small group [25] of SGA
cases have these velocities been studied when growth pathology could have been
present (21). However, a recent investigation of 184 SGA singletons identified 53
Normal and 73 Growth Restricted cases in which concordance between 3rd
trimester growth status and neonatal outcomes was observed (10). Our
investigation characterizes and compares 2nd trimester growth velocities of these
two groups with each other and in relationship to fetuses having normal neonatal
growth outcomes. Our principal objective was to determine if these growth
velocities could be considered appropriate estimates of growth potential in SGA
Using Individualized Growth Assessment [IGA], 126 cases were divided into 53
having normal growth [SGA N] and 73 having third trimester growth restriction
[SGA GR], as identified with the Fetal Growth Pathology Score {FGPS1}
[HC,AC,FDL,EWT] (10). Neonatal growth outcomes, evaluated using the average
negative, pathological Growth Potential Realization Index {av –pGPRI} [WT, HC,
CHL] (10, 21), were all correspondingly normal or growth restricted (10).
For comparisons with SGA singletons, 2nd trimester growth data from 118
singletons with normal neonatal growth outcomes [NNGO], based on a
multivariable, modified Neonatal Growth Assessment Score which corrected for
differences in birth age and growth potential (24), were used in this investigation
(9). These data were obtained as part of a prospective, longitudinal study in a
single institution where all ultrasound measurements were made by one research
ultrasonographer or MFM specialist. Details concerning the selection of this
sample can be found in a previous publication (9).
Fetal Age Determination
Crown-rump length measurements [before 12 weeks] or a composite age parameter
[BPD, HC, AC, FDL] measured before 16 weeks, MA were used to estimate fetal
age as previously described (10).
Assessment of Fetal Size Parameters
Ultrasound size measurements [BPD, HC, AC, FDL] were made between 14 and
28 weeks, MA, using methods previously described (10). In the SGA N Group, the
number of scans had a median of 3, with a 100% range of 2 to 5. For the SGA GR
Group, the median number was 3 in all specific SGA Patterns subgroups, with a
100% range of 2 to 4 [exception {Pattern 2}:2 to 5]. The three unclassifiable cases
had a median of 4 scans with a 100% range of 2 to 5. The ultrasound data used in
this study were obtained under conditions similar to those used clinically.
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Abnormal growth patterns have been investigated previously in the growth
restricted group (22). Five distinct patterns, designated Patterns 1-5, and
Unclassifiable, were identified in the 3rd trimester [SGA Patterns Group]. For this
study, the 73 SGA GR cases were initially subdivided into the six SGA Patterns
Data Analysis
Linear Regression
Measurements of specific anatomical parameters in each fetus were used in linear
regression analyses to obtain estimates of parameter growth velocities in the 2nd
trimester. The validity of assumed linear model was evaluated using the coefficient
of determination [R2]. R2 values were available in 43/53 [81.1%] of SGA N Group
cases. In the 73 SGA GR Group cases, R2 values were available in 23/27 [85.2%]
Descriptive statistics were obtained for the four parameters in the six growth
restriction pattern subgroups. Because of the small sample sizes, Kruskal-Wallis
one-way analysis was used to compare the R2 values for each anatomical parameter
in the six Patterns subgroups. The similarities between all parameters in all
Patterns subgroups [Table 1] justified pooling the subgroups to give a single SGA
GR Group. The R2 values for each anatomical parameter in the SGA N Group {43
cases}, the SGA GR Group {60 cases} and the NNGO Group {118 cases} [Table
2] were compared using ANOVA.
2nd Trimester Growth Velocity
A secondary analysis determined the number of R2 values below 95% for each of
the four anatomical parameters in the Pattern Groups, the SGA N Group, the SGA
GR Group and the NNGO Group.
The sequence of statistical analyses described for the R2 values was repeated with
2nd trimester growth velocity data obtained with the Individualized Growth
Assessment Program [iGAP;]. However, the SGA N
Group contained 53 cases and the SGA GR Group 73 cases due to inclusion of
cases where the growth velocities were calculated directly from two measurements.
If significant differences were found with ANOVA, pair-wise comparisons of the
main three groups were carried out using the t-test [p <0.05} with Bonferroni
adjustment of the p-value [p<0.017] in multiple comparisons.
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of the Pattern 1 cases, 14/20 [70%] of the Pattern 2 cases, 8/9 [88.9%] of the
Pattern 3 cases, 7/8 [87.5%] of the Pattern 4 cases, 6/6 [100%] of the Pattern 5
cases and 2/3 [66.7%] of the unclassifiable cases. The missing R2 values were
those cases with only 2 scans in the 2nd trimester. For the NNGO Group, R2 values
were available in all 118 cases.
A secondary analysis compared growth velocities to the lower limits of their
respective reference ranges [BPD: 0.25 cm/wk; HC:0.90 cm/wk; AC: 0.90 cm/wk;
FDL:0.20 cm/wk] (9). These comparisons were carried out using the Abnormal
Growth Velocity Scores [AGVS] obtained with iGAP software. The AGVS is a
statistic used to quantify growth pathology in the 2nd trimester by comparison of
measured growth velocities to their 95% reference ranges, obtained in fetuses with
normal neonatal growth outcomes (9). This statistic is calculated by comparing the
measured 2nd trimester growth velocity to the appropriate reference range and
determining if it is within or outside this range. If the velocity is within the
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Comparisons of Growth Velocities to Lower Reference Range Boundaries
Comparison of 2nd trimester growth rates to their respective reference range lower
boundaries (9) in the NNGO Group revealed only 6 of 478 [1.3%] values below
these boundaries [BPD: 5; HC: 0; AC:0; FDL: 1]. The corresponding differences
from the boundaries were all -0.02 cm/wk with one exception [-0.10].
In the SGA GR Group, there were 30/292 [10.3%] values below the boundaries
[BPD: 6; HC:7; AC: 15; FDL: 2]. The corresponding differences from the
boundaries were -.01[9 values], -.02 [4 values], -.03[3 values], -.04[2 values],
-.05[2 values], -.07[4 values], -.08 [2 values],-.09[2 values], -.15, -.17 cm/wk.
Primary Findings
In the SGA Patterns subgroups, Pattern 1 had 18/108 [16.7%] values below the
boundaries, Pattern 2 had 6/80[7.6%], Pattern 3 had 1/36 [2.8%], Pattern 4 had
4/32 [12.5%], Pattern 5 had 2/24 [8.3%] and Pattern Unspecifiable had 1/12
Constant growth velocity in the 2nd trimester is an important part of the rationale
for proposing the use of these velocities as measures of fetal growth potential
[Appendix]. Second trimester growth velocities have been previously evaluated in
SGA singletons but the sample was small, 10 SGA Normals and 15 SGA Growth
Restricted (21) vs. 53 and 73 in the current study. Our investigation represents the
first comprehensive evaluation of 2nd trimester growth in a large SGA sample
where concordant fetal and neonatal growth evaluations provide the basis for
subdividing the sample into normal and growth restricted subgroups. The latter was
further subdivided based on the pattern of growth restriction.
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In the SGA N Group, there were 8/212 [3.8%] values below the boundaries [BPD:
2; HC: 1; AC:3; FDL:2]. The corresponding differences from the boundaries were
-.06, -.05, -.01, -.05, -.06, -.08, -.01, -.03 cm/wk.
As seen in Table 1, very strong evidence for linear growth [and hence constant
growth velocities] in the 2nd trimester was found in all groups and subgroups of the
SGA sample. These results were very similar to those found previously under ideal
research conditions (9) although the SGA data were obtained in a more clinical
setting. Average and median R2 values were in the 98-99% range and the
A more detailed examination of the growth velocities themselves [Table 2] indicate
that fetuses in the SGA Group, on average, are growing more slowly than those
with normal neonatal growth outcomes [exception: FDL] even in the 2nd trimester.
This suggests a lower growth potential, which may or may not be due to pathology
occurring in the first trimester. Within the SGA Group, only the AC had a smaller
growth velocity, on average, in the growth restricted subgroup. This anatomical
parameter also had the largest number of growth velocity values just below the
lower limit of the reference range. These data suggest that even in the 2nd trimester
there is some evidence of impending growth abnormalities later in pregnancy in
certain individuals. However, in the SGA Group, 466/504 [92.5% {Normal: 96%;
Growth Restricted: 90%}] of the second trimester growth velocities were within
their 95% reference ranges.
The issue of 2nd trimester growth velocities just below the lower boundaries of
their 95% reference ranges has been discussed but not investigated in detail (10).
Since by definition, some of these growth velocities could be normal, further study
was warranted. Such growth velocities were found in all three major groups but
only the SGA Growth Restricted Group had more than 4% of such values [10.3%].
With two exceptions [AC: 0.15, 0.17 cm/wk] all differences were 0.09 or less
cm/wk and present in all anatomical parameter categories. Among the different
growth restriction patterns only Pattern 1[growth abnormality increasingly worse
during pregnancy] had a somewhat high number [16.7%] of these growth velocities
and they were mainly in AC. These results suggest that differences from the lower
boundary of 0.08 cm/wk [rather than 0.09 cm/wk (10)] or less could be used to
identify growth velocities that might still be found in normally growing fetuses.
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proportions below 95% were less than 4% in all three major groups. Special
research conditions do not appear to be necessary for obtaining reasonable
estimates of 2nd trimester growth velocities. However, as intra- and inter-observer
measurement errors can significantly affect these biometric parameters (25),
careful measurements are necessary to avoid generating inaccurate individualized
standards. This effect can be particularly significant if only two measurements are
used in growth velocity calculations. Use of regression analysis mitigates this
problem but at least three measurements are required.
Previous Studies
Second trimester growth velocities [BPD, HC, AC, FDL] of individual fetuses in
Only four publications provide information on the variability of 2nd trimester
growth velocities for groups of normal fetuses [cross-sectional data]. Fascina et al
(11) reported mean velocities for BPD, HC and AC of 0.40 to 0.30 cm/wk, 1.30 to
1.10 cm/wk and 1.20 to 1.00 cm/wk, respectively, during the 14-26 week, MA,
period in 30 fetuses. For BPD and FDL, Gudihard-Costa et al (12) gave mean
velocities of 0.39 to 0.32 cm/wk and 0.33 to 0.25 cm/wk, respectively, during the
14-26 wk, MA, period in a study of 3433 cases. Deter and Harrist (13), using
instantaneous velocities obtained from 20 fetuses, reported mean values for BPD,
HC, AC and FDL of 0.30 to 0.30, 1.40 to 1.10, 1.20 to 1.20, and 0.30 to 0.30
cm/wk, respectively, for this same time period. Finally, Bertino et al (16) presented
graphs of growth velocity Expected Values for BPD, HC, AC and FDL derived
from 238 singletons. From these graphs, the beginning-peak-final growth velocities
for the 14-26 week interval can be extracted. For BPD, the values were
0.34-0.35-0.28 cm/wk. For HC, the values were 1.21-1.29-1.02 cm/wk. For AC,
the values were 0.96-1.06-1.05 cm/wk. For FDL, the values were 0.26-0.29-0.27
cm/wk. The analytical methods used in these studies were quite different, the data
were for groups not individuals and they still contained the effects of uncorrected
differences in growth potential [except for the study of Deter and Harrist (13)].
However, the consistency of 2nd trimester growth velocities [except perhaps for
HC] provides additional support for the concept of relatively constant 2nd trimester
growth velocities.
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SGA cases have only been studied in one previous publication (21). Fifteen of
twenty-five cases had growth restriction and in ten cases growth was normal. Only
1/100 [1%] of the growth velocity measurements [AC] was outside the reference
ranges and the difference from the lower boundary was 0.05 cm/wk.
Strengths and Limitations
A major strength of this investigation is the use of rigorous IGA criteria to identify
individuals in the three main groups studied [NNGO, SGA N, SGA GR]. For the
two SGA groups, concordance between fetal and neonatal growth assessments was
required. This investigation also benefited from the availability of a ‘gold standard’
for 2nd trimester growth assessment in the results provided by the large,
prospective, longitudinal study of fetuses with normal neonatal growth outcomes
(9). A primary limitation was the availability of only two scans in 18.3% of the
cases, and the small number [3-5] in the other 81.7%, for evaluation of 2nd
trimester growth. This study was also limited by the small sample sizes [6 to 27]
in the subgroups of the SGA Patterns Group. Such small samples restrict the
reliability of our results.
The use of IGA requires a period of normal growth to establish individualized
standards. The results of this study indicate that even for fetuses with subsequent
evidence of growth restriction, 2nd trimester growth is essentially normal. This
permits the use of IGA in at risk pregnancies and may allow detection of growth
restriction in its earliest stages when better therapeutic options could be
Second trimester growth in individual, singleton fetuses suggests that the growth of
the BPD, HC, AC and FDL is quite linear, indicating a constant growth velocity
during this period of pregnancy. Similar results were found in fetuses at risk for
growth restriction, both those who later developed this condition and those who did
not. However, fetuses who were SGA at birth grow more slowly than those who
are not, suggesting a difference in growth potential, although 92.5% of these
growth velocities were within their 95% reference ranges. Different patterns of
growth restriction appear to have similar 2nd trimester growth. In most fetuses at
risk for growth restriction, 2nd trimester growth velocities can be considered
appropriate measures of growth potential for use in IGA.
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Clinical Significance
Rose Torno Chair at Mount Sinai Hospital, University of Toronto, to Professor
John Kingdom. This research was supported (in part) by the Perinatology Research
Branch, Division of Intramural Research, Eunice Kennedy Shriver National
Institute of Child Health and Human Development, NIH, DHHS. R. Romero
contributed to this work as part of his official duties as an employee of the United
States Federal Government. None of the other authors have disclosed a conflict of
Can the Growth Potential of Individual Fetuses be Measured?
Fetal growth potential is a concept [latent variable (26)] that does not have a
generally accepted definition. To measure such a quantity, it is necessary to choose
something to represent the concept [observable variable]. This first requires a
definition of the secondary latent variable, growth, which is usually defined as the
change in size of an anatomical parameter with age (14). This definition indicates
that there are multiple ‘growth potentials’, one for each anatomical parameter and
specific measure of size. Change of size with age is commonly called ‘growth
velocity’ (14).
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Previous definitions of fetal growth potential have been limited to birth weight (3)
or skeletal parameters (6). Expected weights at birth were calculated by regression
analysis after adjusting for up to 19 known birth weight determinants (3,27). This
approach only accounted for, at most, 36% of the weight variability (27). The
growth of skeletal parameters was studied longitudinally in a multi-national,
proscriptive sample which minimized growth abnormality risk factors and
optimally supported fetal growth (6). The observed empirical size parameter
variability in this sample was taken as measures of growth potential. This approach
tacitly assumes that normally growing fetuses follow group percentile lines, an
assumption not supported in recent longitudinal studies (20).
>Second trimester growth velocities are measures of change in size with time.
not size alone, so are the most appropriate growth measurements (8).
>Second trimester growth velocities are empirical measures that reflect the
effects of both known and unknown determinants of growth (27).
> Second trimester growth velocities can be measured at a time when fetal
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In IGA, a different approach has been used. The observable variables for fetal
growth potential were the individual, second trimester growth velocities of nine
size parameters studied in fetuses with normal neonatal growth outcomes (9). They
were chosen for the following reasons:
nutritional requirements are low [as evidenced by similar 2nd trimester growth
in singletons, twins and triplets (28)], thus reflecting the effects of intrinsic
determinants rather than the environment provided by the
> Second trimester growth velocities of 1D, 2D and 3D anatomical
parameters do not change appreciably during this period of pregnancy,
provided the 2D and 3D measurements are appropriately transformed (8).
>Second trimester growth velocities can specify Rossavik size models that
accurately predict 3rd trimester size trajectories and birth characteristics in
fetuses with normal neonatal growth outcomes (9,18).
velocities (9), usually have normal values in fetuses with subsequent growth
restriction or macrosomia (29,30).
Although no single attribute can definitively establish that the second trimester
growth velocity represents fetal growth potential, the set of attributes given above
are consistent with a logical definition of this important biological characteristic of
the growing fetus.
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> Rossavik model coefficient c values, predicted from second trimester growth
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