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Growth Curves Article
Growth Curves Article
e214 OLSEN et al
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ARTICLES
Intrauterine growth curves are the nations, prenatal ultrasound, and to the relationships in the following
standard for assessing the growth of postnatal physical examinations; in formulas: z ⫽ [(X/M)L ⫺ 1]/LS, where X
preterm infants1 and are widely used completed weeks) gender, and race is the measured value of weight (in
in the NICU setting. Intrauterine (using maternal race). kg), length, or HC; and Centile ⫽ M(1 ⫹
curves, which are based on cross- Infants were excluded for missing LSZ)1/L, where Z is the z score that cor-
sectional birth data, differ from longi- weight, length, or head circumference responds to a given percentile. The
tudinal postnatal curves2–6 in that (HC); unknown gender; and factors curves were developed so that the re-
these illustrate “ideal” or fetal growth with a known or suspected negative sulting z scores follow a normal distri-
versus actual growth of preterm in- impact on intrauterine growth (eg, bution and then were smoothed and
fants over time, respectively. Newer in- multiple births, congenital anomalies, converted to percentiles for clinical
trauterine growth curves7–14 have been mortality before discharge). These use.
published to improve on earlier data were divided into male and fe- Several techniques were used to as-
curves,3,15–18 by using more current, male because of differences in birth sess goodness of fit for each curve.
larger, and more diverse samples of size found in the current sample20 as Worm plots25 were used for visual in-
infants; however, these more recent well as in a previous study of Pedia- spection of the fit of the smoothed
curves still have limitations, such as the trix data19 and other data sets.11,12,16 curves, and the “best” version was
lack of length- and head circumference- confirmed by visual inspection of the
Infants with physiologically improba-
for-age curves to accompany the weight- empirical percentiles (on the basis of
ble growth measurements (“extreme
for-age curves,7,8,10,12,14 different sam- these raw data) superimposed on the
outliers”) were excluded from the
ples for growth measurements (eg, smoothed curves. Z scores were calcu-
gender-specific samples. As in previ-
different sample of infants for weight- lated for each infant in the curve sam-
ous growth studies,21,22 extreme outli-
for-age than length-for-age),9 and/or
ers were defined as values ⬎2 times ples by using the aforementioned cal-
the curves are based on samples of culations and grouped by GA. Because
the interquartile range (25th to 75th
infants from outside the United standard percentile curves such as
percentiles) below the first quartile
States.9,11 The goals for this study were ours are based on a normal distribu-
and above the third quartile for each
to develop a new set of growth curves tion of z scores, the overall mean and
GA.23 For each gender, these data were
for the assessment of weight, length,
randomly divided into 2 subsamples: SD for the calculated z scores for the
and head circumference of preterm in-
the “curve samples” were used to cre- sample should be 0.0 ⫾ 1.0. Inspection
fants in the NICU setting using a con-
ate the curves, and the “validation of the calculated z score distributions
temporary, large, racially diverse US
samples” were used to validate the by GA was used to determine whether
sample; validate these curves; and
resultant curves. SAS SURVEYSELECT the curves fit these data well at all GAs.
compare them with 1 of the older but
procedure was used to create strati-
still commonly used growth curves in Curve Validation
fied random samples; gender-specific
NICUs, the Lubchenco curves.15,16
stratification was by GA, race, and The new growth curves were validated
METHODS state in which the birth hospital was by using gender-specific validation
This study used a deidentified, cross- located. samples. For each growth measure, z
sectional sample of birth data from Pe- scores, SDs, and confidence intervals
Curve Creation (CIs) for all validation infants were cal-
diatrix Medical Group, Inc (data collec-
tion details previously summarized19). Gender-specific weight-, length-, and culated using the LMS parameters
The sample included 391 681 insured HC-for-age intrauterine curves were from the new growth curves for each
and uninsured infants aged 22 to 42 created in this study. LmsChartMaker GA. Means and CIs were compared
weeks at birth born in 1 of 248 hospi- Pro 2.324 was used to create smoothed with 0, and SDs were compared with 1
tals within 33 US states (1998 –2006). percentile curves for the 3rd, 10th, (using an adjusted ␣ of .003 for 19
Available data included birth weight 25th, 50th, 75th, 90th, and 97th percen- comparisons within each gender).
(measured on electronic scale to near- tiles from these raw data. Cole’s The new curves were further evaluated
est gram), length and head circumfer- Lambda Mu Sigma (LMS) method esti- by examining the percentage of infants
ence (using measuring tape to nearest mates 3 age-specific parameters: a whose growth measurements fell
millimeter), estimated gestational age Box-Cox power transformation of within the size-for-age categories rou-
(GA; by neonatologist best estimate us- skewness (L), median (M), and coeffi- tinely used in NICUs. By definition,
ing obstetric history, obstetric exami- cient of variation (S) that correspond ⬃10% of a population should be
10th
50th
3500 3rd
25th 45
Centimeters
3000 10th
3rd 40
2500
97th
90th
75th
35 50th
2000
25th
10th
3rd
1500 30
Head Circumference
1000
25
500
23 25 27 29 31 33 35 37 39 41 20
Gestational Age, weeks
23 25 27 29 31 33 35 37 39 41
Gestational Age, weeks
C D 97th
Weight, gm 97th 90th
4500 55
75th
90th Length
50th
75th 25th
4000 50
10th
50th 3rd
3500
25th 45
Centimeters
10th
3000
3rd
40
2500 97th
90th
75th
35 50th
2000 25th
10th
3rd
1500 30
Head Circumference
1000
25
500
23 25 27 29 31 33 35 37 39 41 20
Gestational Age, weeks
23 25 27 29 31 33 35 37 39 41
Gestational Age, weeks
FIGURE 1
New gender-specific intrauterine growth curves for girls’ weight for age (A), girls’ length and HC for age (B), boys’ weight for age (C), and boys’ length and
HC for age (D). Of note, 3rd and 97th percentiles on all curves for 23 weeks should be interpreted cautiously given the small sample size; for boys’ HC curve
at 24 weeks, all percentiles should be interpreted cautiously because the distribution of data is skewed left. Adapted from Groveman.20
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ARTICLES
⬍10th percentile (small for GA [SGA]), TABLE 1 Female Birth Weight, Length, and HC Percentiles by GA
⬃80% between the 10th and 90th per- GA, wk n Birth Size Percentile
centiles (appropriate-for-GA [AGA]), Mean SD 3rd 10th 25th 50th 75th 90th 97th
and ⬃10% ⬎90th percentile (large- Weight, g
for-GA [LGA]). 23 133 587 80 NAa 477 528 584 639 687 NAa
24 438 649 89 464 524 585 651 715 772 828
25 603 738 121 511 584 657 737 816 885 953
Comparison of Lubchenco Curves
26 773 822 143 558 645 732 827 921 1004 1085
With New Curves and Validation 27 966 934 168 615 719 822 936 1047 1147 1244
Data Set 28 1187 1058 203 686 807 928 1061 1193 1310 1425
29 1254 1199 226 778 915 1052 1204 1354 1489 1621
The new curves were also compared 30 1606 1376 246 902 1052 1204 1373 1542 1693 1842
with the Lubchenco curves15,16 because 31 2044 1548 271 1033 1196 1361 1546 1731 1897 2062
32 3007 1730 300 1177 1352 1530 1731 1933 2116 2297
these are commonly used in NICUs and 33 4186 1960 328 1356 1545 1738 1956 2178 2379 2580
met the following a priori criteria: in- 34 5936 2194 357 1523 1730 1944 2187 2434 2661 2888
cluded curves for weight-, length-, and 35 5082 2420 440 1626 1869 2123 2413 2711 2985 3261
36 4690 2675 514 1745 2028 2324 2664 3015 3339 3667
HC-for-age, which were created from
37 4372 2946 551 1958 2260 2575 2937 3308 3651 3997
the same sample; and the curves were 38 5755 3184 512 2235 2526 2829 3173 3525 3847 4172
based on US data. The validation infants 39 5978 3342 489 2445 2724 3012 3338 3670 3973 4276
40 5529 3461 465 2581 2855 3136 3454 3776 4070 4363
(as a whole and stratified by GA and GA
41 1906 3546 477 2660 2933 3214 3530 3851 4142 4433
groups 23–26 weeks, 27–31 weeks, Length, cm
32–36 weeks, and 37– 41 weeks) were 23 133 29.9 1.8 NAa 27.7 28.7 29.9 31.0 31.9 NAa
24 438 31.0 1.7 27.5 28.7 29.8 31.1 32.3 33.3 34.3
classified as SGA or LGA by using the Lub-
25 603 32.3 2.0 28.3 29.7 31.0 32.3 33.6 34.8 35.9
chenco curves. The amount of misclassi- 26 773 33.4 2.2 29.2 30.7 32.1 33.6 35.1 36.3 37.4
fication was summarized, and a likeli- 27 966 35.0 2.3 30.2 31.9 33.4 35.0 36.6 37.9 39.1
hood ratio 2 was calculated to assess 28 1187 36.4 2.5 31.4 33.1 34.8 36.5 38.1 39.5 40.8
29 1254 37.8 2.7 32.8 34.6 36.3 38.0 39.7 41.2 42.5
statistical significance of differences 30 1606 39.6 2.6 34.3 36.0 37.7 39.5 41.3 42.7 44.1
with a Bonferroni adjusted ␣. 31 2044 40.9 2.6 35.7 37.5 39.2 41.0 42.7 44.1 45.5
32 3007 42.1 2.6 37.1 38.9 40.6 42.3 44.0 45.5 46.9
Statistical Analysis 33 4186 43.7 2.6 38.6 40.3 41.9 43.7 45.4 46.9 48.3
34 5936 45.0 2.6 39.8 41.5 43.2 45.0 46.7 48.2 49.7
The worm plots were generated by us- 35 5082 46.0 2.7 40.9 42.6 44.3 46.2 48.0 49.5 51.0
ing S-PLUS 8.0, and SAS 9.1 was used 36 4690 47.2 2.8 42.0 43.7 45.5 47.4 49.2 50.8 52.3
37 4372 48.4 2.8 43.2 44.9 46.6 48.5 50.3 51.9 53.4
for all other statistics. 38 5755 49.5 2.6 44.4 46.1 47.7 49.5 51.2 52.7 54.2
39 5978 50.1 2.5 45.3 46.9 48.5 50.2 51.9 53.3 54.7
RESULTS 40 5529 50.7 2.4 46.1 47.6 49.1 50.8 52.4 53.8 55.1
41 1906 51.3 2.4 46.7 48.2 49.7 51.3 52.8 54.2 55.5
From the 391 681 infants, exclusions HC, cm
were made for missing growth data 23 133 20.8 1.2 NAa 19.5 20.1 20.9 21.6 22.2 NAa
(n ⫽ 31 319; 8% of total sample), un- 24 438 21.7 1.1 19.6 20.3 21.0 21.8 22.5 23.2 23.8
known gender (n ⫽ 215; 0.05%), factors 25 603 22.7 1.2 20.4 21.1 21.9 22.7 23.4 24.1 24.8
26 773 23.5 1.2 21.2 22.0 22.7 23.6 24.4 25.1 25.9
that negatively affect growth (n ⫽ 27 966 24.5 1.3 21.9 22.8 23.6 24.5 25.4 26.2 27.0
95 962; 24.5%), and physiologically im- 28 1187 25.5 1.5 22.7 23.7 24.6 25.5 26.5 27.3 28.1
probable growth measurements (1.6% 29 1254 26.5 1.5 23.6 24.6 25.5 26.5 27.5 28.4 29.2
30 1606 27.5 1.5 24.6 25.6 26.5 27.5 28.5 29.4 30.2
of total sample: n ⫽ 3578 or 0.9% boys; 31 2044 28.4 1.5 25.5 26.5 27.4 28.4 29.4 30.3 31.1
n ⫽ 2752 or 0.7% girls). The final sample 32 3007 29.3 1.5 26.5 27.4 28.3 29.3 30.3 31.2 32.0
included 257 855 infants (57.2% male) 33 4186 30.2 1.5 27.3 28.3 29.2 30.2 31.2 32.1 33.0
34 5936 31.1 1.6 28.1 29.1 30.1 31.1 32.2 33.1 34.0
with a race distribution of 50.6% white, 35 5082 31.9 1.6 28.8 29.8 30.8 31.9 33.0 34.0 34.9
15.7% black, 24.4% Hispanic, and 9.3% 36 4690 32.6 1.7 29.4 30.5 31.5 32.7 33.8 34.8 35.8
other, similar to US birth data available 37 4372 33.3 1.7 30.1 31.1 32.2 33.3 34.4 35.4 36.3
38 5755 33.8 1.6 30.7 31.7 32.7 33.7 34.8 35.7 36.7
from National Vital Statistics System
39 5978 34.0 1.5 31.1 32.0 33.0 34.0 35.1 36.0 36.9
2005 (55.1% white, 14.1% black, 23.8% 40 5529 34.2 1.5 31.4 32.3 33.3 34.3 35.3 36.1 37.0
Hispanic, and 7.0% other). The “curve 41 1906 34.5 1.5 31.7 32.6 33.5 34.5 35.5 36.3 37.1
samples” included 74 390 boys and Adapted from Groveman.20
a Not available because of small sample size.
55 721 girls, and the “validation sam-
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ARTICLES
TABLE 3 Gender-Specific Weight-, Length-, and HC-for-Age Growth Curves L, M, and S Parameters tion for each measure within each gen-
GA, wk Weight-for-Age Curve Length-for-Age Curve HC-for-Age Curve der, and percentiles within expected
L Curve M Curve S Curve L Curve M Curve S Curve L Curve M Curve S Curve ranges. These indicate that the curves
Value Value Value Value Value Value Value Value Value are a good fit to the validation samples
Female growth and would be expected to show a sim-
curves
23 1.195 0.584 0.140 1.613 29.861 0.055 1.338 20.863 0.052
ilar good fit to the population from
24 1.180 0.651 0.149 1.799 31.074 0.058 1.412 21.759 0.051 which the samples were drawn.
25 1.161 0.737 0.159 2.005 32.323 0.062 1.500 22.667 0.052
26 1.140 0.827 0.169 2.234 33.638 0.065 1.599 23.584 0.053
The percentage of the validation sam-
27 1.116 0.936 0.178 2.395 35.047 0.067 1.685 24.541 0.054 ple classified as SGA or LGA for the
28 1.087 1.061 0.185 2.396 36.522 0.068 1.740 25.529 0.056 group overall (⬃10% SGA and ⬃10%
29 1.054 1.204 0.186 2.231 38.041 0.068 1.771 26.525 0.055
LGA), for individual GAs (⬃10% for
30 1.015 1.373 0.182 2.125 39.545 0.066 1.778 27.507 0.054
31 0.975 1.546 0.177 2.217 40.961 0.063 1.774 28.433 0.052 each), and for GA groups was deter-
32 0.930 1.731 0.172 2.172 42.334 0.061 1.754 29.333 0.050 mined. For GA groups, boys and girls
33 0.878 1.956 0.167 1.938 43.701 0.059 1.720 30.241 0.050 were combined when calculating CIs
34 0.827 2.187 0.166 1.784 44.978 0.058 1.677 31.126 0.050
35 0.786 2.413 0.181 1.746 46.167 0.058 1.647 31.944 0.051 for the percentage of SGA/LGA as a re-
36 0.764 2.664 0.192 1.750 47.356 0.058 1.629 32.675 0.052 sult of small sample size at the
37 0.771 2.937 0.185 1.809 48.501 0.056 1.613 33.289 0.050 younger GAs. In all cases, the CIs and
38 0.796 3.173 0.163 1.840 49.476 0.052 1.601 33.742 0.047
39 0.821 3.338 0.146 1.883 50.214 0.050 1.597 34.040 0.045 percentages were consistent with
40 0.841 3.454 0.137 1.922 50.788 0.047 1.595 34.273 0.043 ⬃10%, as would be expected if the
41 0.855 3.530 0.134 1.958 51.271 0.046 1.595 34.497 0.042 curves were correctly classifying in-
Male growth
curves
fants. Figure 4 shows an example of 1
23 1.317 0.621 0.136 1.608 30.282 0.057 1.450 21.349 0.049 of these analyses for GA groups.
24 1.305 0.690 0.142 1.748 31.543 0.059 1.510 22.246 0.049
25 1.289 0.780 0.150 1.889 32.862 0.062 1.570 23.174 0.050
Comparison of Lubchenco Curves
26 1.270 0.890 0.158 2.029 34.265 0.064 1.630 24.164 0.051
27 1.248 1.009 0.165 2.159 35.732 0.065 1.685 25.178 0.052 With New Curves and Validation
28 1.224 1.141 0.171 2.264 37.221 0.066 1.727 26.145 0.052 Data Set
29 1.196 1.280 0.174 2.335 38.669 0.065 1.750 27.062 0.052
30 1.162 1.443 0.174 2.367 40.110 0.064 1.756 27.987 0.052 The new gender-specific curves were
31 1.122 1.631 0.171 2.357 41.555 0.062 1.747 28.935 0.052 plotted with the unisex Lubchenco
32 1.075 1.829 0.167 2.314 42.974 0.060 1.734 29.855 0.051 curves (gender-specific US curves
33 1.021 2.057 0.164 2.244 44.368 0.058 1.727 30.758 0.051
34 0.968 2.285 0.163 2.163 45.658 0.057 1.729 31.630 0.051 not available) for comparison. Figure
35 0.917 2.527 0.171 2.074 46.876 0.057 1.736 32.448 0.051 5 presents the weight-for-age curves
36 0.873 2.792 0.177 1.973 48.102 0.057 1.744 33.212 0.051 as an example of these comparisons.
37 0.839 3.056 0.171 1.866 49.270 0.055 1.748 33.869 0.050
38 0.814 3.306 0.158 1.769 50.249 0.052 1.750 34.358 0.048 Generally, the new curves had lower
39 0.796 3.469 0.146 1.689 51.007 0.049 1.751 34.638 0.046 average weights, lengths, and HC at
40 0.785 3.579 0.140 1.626 51.612 0.047 1.752 34.832 0.045 younger GAs than the Lubchenco
41 0.776 3.666 0.136 1.572 52.122 0.046 1.752 35.033 0.044
curves until 30 to 36 weeks; the new
Adapted from Groveman.20 The LMS method estimates 3 age-specific parameters: a Box-Cox power transformation of
skewness (L), median (M), and coefficient of variation (S). curves had higher average growth
measurements at older GAs. When
sentially 0, and the z scores exhibited a length and HC z scores were approxi- the validation samples were catego-
Gaussian distribution. mately normally distributed. The only rized as SGA/AGA/LGA by using the
Similar results were observed when exception was that HC z scores for in- Lubchenco curves, we found a statis-
these data were stratified by GA for fants ⬍26 weeks approached a nor- tically significant difference for each
which all but 1 of the means were ⬍0.1 mal distribution except for 24-week GA, GA group, and the group as a
away from 0. Figure 2 shows an exam- boys, which showed a slight skew with whole (all P ⬍ .0001). Table 4 presents
ple of this, illustrating that all CIs in- a mean of 0.02, a median of 0.22, and the overall comparisons (boys and girls
clude 0. In addition, the age-specific z skewness of 0.24. combined). Overall, the percentage of
scores had means and medians within Figure 3 shows the gender-specific SGA infants was underestimated by the
ⱕ0.02 of each other, and each had a percentile distributions in the valida- Lubchenco curves except for younger
skewness of ⱕ0.009. Weight z scores tion samples by using the curve LMS girls (approximately ⱕ36 weeks), for
were always normally distributed, and values, illustrating a normal distribu- whom it was more likely to be overesti-
0.1
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ARTICLES
A B
Weight, grams Weight, grams
4500 4500
90th
90th 4000
4000
3000 3000
10th
th
10
2500 2500
2000 2000
1500 1500
1000 1000
500 500
24 26 28 30 32 34 36 38 40 24 26 28 30 32 34 36 38 40
Gestational Age, Weeks Gestational Age, Weeks
FIGURE 5
New weight-for-age gender-specific curves (solid line) for girls (A) and boys (B) compared with Lubchenco unisex curves (dashed line; start at 24 weeks16).
Adapted from Groveman.20
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New Intrauterine Growth Curves Based on United States Data
Irene E. Olsen, Sue A. Groveman, M. Louise Lawson, Reese H. Clark and Babette S.
Zemel
Pediatrics; originally published online January 25, 2010;
DOI: 10.1542/peds.2009-0913
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Downloaded from pediatrics.aappublications.org at Virginia Hosp Ctr Arlington on August 16, 2015
New Intrauterine Growth Curves Based on United States Data
Irene E. Olsen, Sue A. Groveman, M. Louise Lawson, Reese H. Clark and Babette S.
Zemel
Pediatrics; originally published online January 25, 2010;
DOI: 10.1542/peds.2009-0913
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located on the World Wide Web at:
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