Extrauterine Growth Restriction Remains a Serious Problem in Prematurely

Born Neonates
Reese H. Clark, Pam Thomas and Joyce Peabody
Pediatrics 2003;111;986

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Extrauterine Growth Restriction Remains a Serious Problem in

Prematurely Born Neonates
Reese H. Clark, MD*; Pam Thomas, RN*; and Joyce Peabody, MD*
ABSTRACT. Background. Poor growth is a common
problem in premature neonates and may be associated
with neurodevelopmental delay.
Objective. To evaluate the incidence of extrauterine
growth restriction (growth values <10th percentile of
intrauterine growth expectation based on estimated postmenstrual age in premature (2334 weeks estimated gestational age) neonates at the time they are discharged
from the hospital.
Design/Methods. Using a database formed from a
computer-assisted tool that generates clinical progress
notes and discharge summaries on neonatal intensive
care unit admissions, we reviewed data on neonates discharged from 124 neonatal intensive care units between
January 1, 1997, and December 31, 2000. We evaluated
neonates who were born between 23 and 34 weeks estimated gestational age without congenital anomalies and
who were cared for at and discharged from the same
hospital. For each patient, we compared the discharge
growth values to the expected values based on our intrauterine growth data and postmenstrual age on the day of
discharge. We defined extrauterine growth restriction as
having a measured growth value (weight, length or head
circumference) that was <10th percentile of the predicted
value. In each specific birth weight and estimated gestational age group, we counted the number of neonates
<10th percentile for each growth parameter and calculated the percentage of patients who had values <10th
percentile at discharge. Using logistic regression, we
evaluated the factors associated with extrauterine growth
restriction for weight, length, and head circumference.
Results. Our sample included 24 371 premature neonates. Data on discharge weight, length, and head circumference was available on 23 970, 17 203, and 20 885
neonates, respectively. The incidence of extrauterine
growth restriction was common (28%, 34%, and 16% for
weight, length, and head circumference, respectively).
For each growth parameter, the incidence of extrauterine
growth restriction increased with decreasing estimated
gestational age and birth weight. Factors independently
associated with extrauterine growth restriction were male
gender, need for assisted ventilation on day 1 of life, a
history of necrotizing enterocolitis, need for respiratory
support at 28 days of age, and exposure to steroids during
the hospital course.
Conclusions. Extrauterine growth restriction remains
a serious problem in premature neonates especially for
neonates who are small, immature, and critically ill.
From *The Pediatrix-Obstetrix Center for Research and Education, Pediatrix
Medical Group, Inc, Sunrise, Florida; and Duke University Medical Center,
Durham, North Carolina.
Received for publication May 3, 2002; accepted Oct 3, 2002.
Reprint requests to (R.H.C.) Pediatrix Medical Group, Inc, 1301 Concord
Terr, Sunrise, FL 33323-2825. E-mail: reeseclark@pediatrix.com
PEDIATRICS (ISSN 0031 4005). Copyright 2003 by the American Academy of Pediatrics.

986

Pediatrics 2003;111:986 990; neonate, growth, retrospective clinical study.

ABBREVIATION. NICU, neonatal intensive care unit.

n premature neonates, achieving recommended

dietary intakes takes time and is rarely maintained throughout the duration of hospitalization.
Nutrient deficits accrue and are rarely replaced. The
term extrauterine growth restriction is descriptive of
stunted growth resulting from severe nutritional deficit during the first weeks of life. Despite some
catch-up growth during the second month of life,
many neonates go home significantly smaller than
expectations based on intrauterine growth rates.
Their nutritional deficit affects not only their weight
but their head circumference and length as well.1
Postnatal growth lag is associated with neurologic
and sensory handicaps and poor school performance.2 This means that neonates who have extrauterine growth restriction may be at risk for longterm medical problems.1
Our objective was to evaluate the incidence of
extrauterine growth restriction (growth values 10th
percentile of intrauterine growth expectation based
on estimated gestational age) in premature (2334
weeks) neonates at the time they are discharged from
the hospital.
METHODS
Research Design
We conducted a retrospective review of an administrative database to describe the growth outcomes of premature neonates at
the time of discharge from neonatal intensive care.

Study Population
Neonates discharged from 124 neonatal intensive care units
(NICUs) managed by Pediatrix Medical Group, Inc between January 1, 1997, and December 31, 2000, who were 23 to 34 weeks
estimated gestational age without congenital anomalies and who
were born at and discharged from the same NICU (N 24 371)
were eligible for inclusion in the study. Data on discharge weight,
length, and head circumference was available on 23 970, 17 203,
and 20 885 neonates, respectively. In our data analysis each of
these 3 groups was evaluated as an independent sample.

Data Collection
Using a database from a computer-assisted tool that generates
clinical progress notes on neonates cared for by Pediatrix Medical
Group, Inc., we reviewed data on birth weight, estimated gestational age (this represents the best estimate based on both obstetric
data and neonatal examination), gender, Apgar scores at 5 minutes, race (choices in database are white, black, Hispanic, Native
American and Asian), use of antenatal steroids, use of postnatal

PEDIATRICS Vol. 111 No. 5 May 2003

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steroids (dexamethasone or hydrocortisone), use of assisted ventilation during the first day of life, use of surfactant, use of respiratory support at 28 days after birth (oxygen, continuous positive
airway pressure, or assisted ventilation), and a diagnosis of necrotizing enterocolitis. We created dichotomous (1/0) variables for
exposure to any type of postnatal steroids (hydrocortisone or
dexamethasone), use of any surfactant, use of respiratory support
at 28 days, and a diagnosis of necrotizing enterocolitis. Neonates
discharged before 28 days were assigned 0 (no support) for the
respiratory variable. We also evaluated data on discharge weight,
length, head circumference, and length of hospital stay. Postmenstrual age was calculated using the estimated gestational age at
birth and the length of hospital stay (ie, estimated gestational age
[length of stay/7]). The database did not include patient identifiers and is maintained as a clinical quality improvement tool.

Definition of Extrauterine Growth Restriction

Extrauterine growth restriction was defined as having a growth
value 10th percentile of intrauterine growth expectation based
on postmenstrual age at the time of discharge to home. We used
our previously published growth curves generated from birth
weights and estimated gestational age at birth to establish expected growth values for neonates discharged at an estimated
gestational age between 33 to 40 weeks.3 Gender-specific values
were used to make the assignment of extrauterine growth restriction. For neonates with an estimated gestational age of 41 to 44
weeks at discharge, we used the gender-specific national standards issued by the Centers for Disease Control and Prevention.4
Each growth parameter (weight, length, and head circumference)
was assessed individually.

Statistical Analysis
We used multivariate logistic regression to identify factors
independently associated with the occurrence of extrauterine
growth restriction for each variable. We evaluated all the variables
in Table 2, which on univariate analysis, were found to be associated with the outcome variable (P .05). We incorporated the
variables found to have significant interactions (P .1) with the
outcome variable in the final logistic regression analysis. Variables
were entered into the model using a stepwise selection (P value for
entry and retention .1). Cases with missing values for any of the
independent variables were excluded from the analysis. The total
number of neonates included in each of the final models is listed
in the tables.

RESULTS

Table 1 shows the sample size and rate of growth

restriction by estimated gestational age at birth. The
most important and significant differences between
neonates who had extrauterine growth restriction
and those who did not were that they had lower
birth weights and were more immature (Tables 2 and
TABLE 1.
Groups

4). The effects of both gestational age and birth

weight are graphically demonstrated in Fig 1. This
graphic shows that neonates born small for gestational age (10th percentile) remain small for gestational age at discharge. In addition, a significant
proportion of neonates who were appropriately
grown for gestational age at birth were discharged
from the hospital with weights 10th percentile for
the gestational age at discharge. Table 3 shows the
sample size and the rate of growth restriction by
postmenstrual age at discharge.
In our multivariate analysis, low birth weight and
immature gestational age were the most important
factors associated with the occurrence of extrauterine
growth restriction (Table 4). Multivariate logistic regression (including gestational age and birth weight)
showed male gender, the need for assisted ventilation on day 1 of life, exposure to steroids during the
hospital course, need for respiratory support on day
28 of age, and a diagnosis of necrotizing enterocolitis
as independent risk factors that increase the odds of
a neonate being labeled as extrauterine growth-restricted. Antenatal steroids appeared to have a small
but significant protective effect. The adjusted odds
ratios and their confidence intervals are listed in
Table 4. As shown by the change in R2 values, adding
risk factors beyond birth weight and gestational age
at birth to the multivariate model did not dramatically improve the performance of the models in predicting extrauterine growth restriction.
DISCUSSION

Our data demonstrate that extrauterine growth

restriction remains a significant problem for prematurely born neonates especially those who develop
significant morbidity or who are treated with postnatal steroids. If we successfully met the nutritional
needs of hospitalized premature infants, we would
expect to find 10% of the premature neonates we
cared for going home with growth values 10th
percentile. In contrast, we found 30% of the neonates
born at 28 weeks estimated gestational age, who
had head circumferences that were appropriate at
birth, went home with head circumferences 10th

The Sample Size and Incidence of Growth Restriction at Discharge in Specific Birth Weight and Estimated Gestational Age

Estimated Number Weight

Weight
Percent
Length
Length
Percent
Head
Head
Percent
Gestational
in
Assessed
10th
Assessed
10th
Circumference Circumference
Age at Birth Sample (Grams) Percentile at
(Centimeters) Percentile at
Assessed
10th
(Weeks)
Discharge
Discharge
(Centimeters) Percentile at
Discharge
23
24
25
26
27
28
29
30
31
32
33
34
Total

100
313
509
708
856
1104
1317
1743
2396
3521
5166
6638
24 371

93
299
488
672
829
1076
1297
1712
2372
3485
5105
6542
23 970

66
191
304
361
384
438
454
534
632
793
1140
1488
6785

71
64
62
54
46
41
35
31
27
23
22
23
28

82
258
418
565
672
882
1055
1393
1842
2565
3510
3961
17 203

76
206
353
407
448
498
499
535
583
641
772
787
5805

93
80
84
72
67
56
47
38
32
25
22
20
34

94
287
475
655
799
1042
1261
1661
2231
3180
4305
4895
20 885

43
134
195
212
211
223
234
252
311
378
534
648
3375

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46
47
41
32
26
21
19
15
14
12
12
13
16

987

TABLE 2.

Description of Study Population and Neonates With Extrauterine Growth Restriction

Characteristic

Number of neonates with growth

values 10th percentile
Estimated gestational age (wk)
Birth weight (kg)
Male gender, n (%)
Apgar score at 5 min; median (range)
Race
Black
Hispanic
White
Other
Exposure to antenatal steroids n %
On assisted ventilation on day 1 of life, n (%)
Surfactant use, n (%)
Exposure to postnatal steroids, n (%)
Respiratory support on d 28, n (%)
Oxygen
Continuous positive airway pressure
Ventilator
Diagnosis of necrotizing enterocolitis, n (%)
Hospital length of stay (d)

Population
Sample

Extrauterine Growth Restriction

Weight 10th
Percentile

Length 10th
Percentile

Head Circumference
10th Percentile

6785 (28)

5805 (34)

3375 (16)

32 3
1.7 0.5
12 961 (53)
9 (010)

31 3*
1.3 0.4*
4044 (60)*
8 (010)

30 3*
1.3 0.4*
3314 (57)*
8 (010)

30 3*
1.3 0.5*
1839 (55)
8 (010)

4131 (17)
4364 (18)
13 494 (55)
2382 (10)
13 824 (57)
6781 (28)
6707 (28)
2701 (11)
4268 (18)
2171 (9)
612 (3)
1485 (6)
528 (2)
32 27

1264 (18)
1270 (19)
3690 (54)
561 (8)
4200 (62)*
2816 (42)*
2610 (38)*
1593 (24)*
2190 (32)*
905 (13)
328 (5)
957 (14)
273 (4)*
47 31*

1243 (21)
974 (17)
3148 (54)
440 (8)
3838 (66)*
2746 (47)*
2598 (45)*
1613 (28)*
2324 (40)*
999 (17)
360 (6)
965 (17)
247 (4)*
52 31*

676 (20)
655 (19)
1786 (53)
258 (8)
2107 (62)*
1529 (46)*
1388 (41)*
969 (29)*
1265 (38)*
459 (14)
179 (5)
627 (19)
176 (5)*
50 34*

* P .01 compared with population sample.

Oxygen support includes nasal cannula oxygen and hood oxygen.

Fig 1. The incidence of extrauterine growth restriction (growth parameter 10th percentile at discharge) in specific birth weight and
gestational age groups. A, Incidence of discharge weight 10th percentile. B, Incidence of discharge length 10th percentile. C, Incidence
of discharge head circumference 10th percentile. Black lines represent the 10th and 90th percentiles base on our previously published
growth curves.3

percentile. This is the only article to report the birth

weight and gestational age-specific occurrence of extrauterine growth restriction at discharge.
Others have reported similar findings. Ehrenkranz
988

et al5 reported that at hospital discharge, most infants born between 24 and 29 weeks of gestation had
not achieved the median birth weight of the reference fetus at the same postmenstrual age. The inci-

EXTRAUTERINE GROWTH RESTRICTION

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TABLE 3.

The Sample Size and Incidence of Growth Restriction at Discharge in Specific Discharge Postmenstrual Age Groups

Postmenstrual
Age at
Discharge
(Weeks)

Weight
Assessed
(Grams)

Weight
10th
Percentile at
Discharge

Percent

Length
Assessed
(Centimeters)

Length
10th
Percentile at
Discharge

Percent

Head
Circumference
Assessed
(Centimeters)

Head
Circumference
10th
Percentile at
Discharge

Percent

34
34
35
36
37
38
39
40
41*
Total

586
2875
7570
6150
3225
1534
850
438
742
23 970

2
88
795
1740
1645
1033
622
319
541
6785

0
3
11
28
51
67
73
73
73
28

355
1839
5001
4566
2500
1250
700
370
622
17 203

18
199
792
1410
1162
847
552
297
528
5805

5
11
16
31
46
68
79
80
85
34

475
2335
6144
5450
3059
1462
816
423
721
20 885

14
134
455
623
836
452
292
187
382
3375

3
6
7
11
27
31
36
44
53
16

* Assessed using Centers for Disease Control and Prevention standard gender-specific growth curves.
TABLE 4.
Adjusted Odds Ratios for Factors Associated With Extrauterine Growth Restriction at Discharge (Correcting for Birth
Weight and Estimated Gestational Age at Birth Using Multivariate Logistic Regression)
Variable

Adjusted Odds Ratio

Weight

Adjusted Odds Ratio

Length

Adjusted Odds Ratio

Head Circumference

Number of patients in final model

Male gender
Exposure to postnatal steroids
Need for respiratory support at 28 d
Diagnosis of necrotizing enterocolitis
Need for assisted ventilation on day 1 of life
Exposure to antenatal steroids
R2 with birth weight and gestational age at
birth only
R2 after adding other variables
Area under receiver operating characteristic
curve for final model

23 639
3.9 (3.64.3)
4.2 (3.64.8)
1.8 (1.62.1)
2.7 (2.13.4)
1.6 (1.52.8)
0.84 (0.810.88)
0.45

16 996
2.2 (2.02.4)
2.3 (1.92.6)
1.6 (1.41.9)
1.8 (1.42.3)
1.2 (1.11.3)
0.92 (0.880.96)
0.35

20 627
1.4 (1.31.5)
2.6 (2.33.0)
1.5 (1.31.7)
2.2 (1.72.7)
1.2 (1.11.4)
0.9 (0.860.94)
0.19

0.48
0.92

0.36
0.87

0.21
0.81

dence of failure-to-thrive (weight 5th percentile for

age/sex) in extremely low birth weight neonates
(400 1000 g) in the Neonatal Research Network cohort was 34% to 45% at 18 months corrected age.6
Postnatal growth lag is associated with neurologic
and sensory handicaps and poor school performance.2 Very low birth weight infants with perinatal
growth failure whose head size is not normal by 8
months of age have significantly poorer growth and
neurocognitive abilities at school age than very low
birth weight children with a normal head size at 8
months.7 The magnitude of the poor growth outcomes we (and others) report demand that we reassess the targets we set for adequate nutrition in
NICUs and after discharge.
Although low birth weight and immature gestational age were the factors that had the most significant effect on the incidence of growth restriction, we
also identified several other factors that appear to
influence growth. All of the factors (gender, need for
respiratory support at birth, necrotizing enterocolitis,
and exposure to postnatal steroids) we identified
may only be surrogate markers for severity of illness.
As described by Ehrenkranz et al,5 premature neonates who require assisted ventilation and have significant adverse events (eg, necrotizing enterocolitis)
are more likely to have poor growth than premature
neonates who do not. This finding is not surprising.
Sick neonates are often fed differently than healthier
infants, have increased metabolic demands, and their

nutritional needs are rarely met, all of which result in

malnutrition and poor growth.
We remain concerned about the potential effects of
postnatal steroids on body and brain growth. Numerous studies now show the profound and lasting
effects that steroids can have on growth of the lungs,
body, and brain.8 12 Our data suggest that neonates
who are exposed to postnatal steroids are at greater
risk of growth failure than those who are not, independent of other risk factors. The association between exposure to postnatal steroids and extrauterine growth restriction remains when multivariate
analysis is used to correct for gestational age, birth
weight, gender, need for assisted ventilation on day
1 of life, need for respiratory support at 28 days after
birth, and a diagnosis of necrotizing enterocolitis.
However, because neonates with chronic lung disease also fail to grow, it is impossible to separate the
effect of chronic lung disease from that of postnatal
steroids. In contrast to the negative effects of postnatal steroids, exposure to antenatal steroids appeared
to have a slight protective effect. It should be emphasized that like most adverse neonatal outcomes, the
most important risk factors associated with extrauterine growth restriction are immaturity and low
birth weight.
There were limitations to our retrospective study
design. Measurements of weight, length and height
were site-specific and not rigorously standardized.
We were missing data on length in a significant

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989

number of our study population and this may have

created a selection bias (ie, patients with abnormal
lengths may have had data reported more often than
patients with normal lengths). In addition, proxies
may not have reflected true severity of illness or the
therapeutic approach. Also, there were site-specific
differences in nutritional approach, which may also
impact the growth restriction incident rates we reported. However, the large size of our population
sample should help decrease these limitations and
help better define the true population event rates,
especially within specific birth weight and gestational age groups.
CONCLUSIONS

We have shown that extrauterine growth restriction remains a common and serious problem for
prematurely born neonates. Although we have made
significant advances in neonatal intensive care, we
need a continued and aggressive effort to study and
define new nutritional strategies that will improve
the nutritional status of prematurely born neonates,
especially the critically ill premature neonate.
APPENDIX
In addition to the authors, the following physicians participated by providing data to the administrative dataset: Harrisburg,
Pennsylvania, K. Lorah; Utica, New York, M. Siriwardena; Boynton Beach, Florida, L. Whetstine; Denver, Colorado, D. Eichorst, J.
Toney; Houston, Texas, R. Rivas, H. Pierantoni, E. ODonnell;
Englewood, Colorado, K. Zarlengo; West Palm Beach, Florida, D.
Kanter; Virginia Beach, Virginia, E. Bollerup; Fredericksburg, Virginia, J. Amin; Spartanburg, South Carolina, V. Iskersky; Watertown, New York, K. Komar; Tarzana, California, J. Banks; Ventura,
California, J. van Houten; Hoboken, New Jersey, S. Mercado;
Stratford, New Jersey, J. Coleman; Trenton, New Jersey, R. Axelrod; Covina, California, G. Martin; Newport Beach, California, L.
Wickham, B. Hannam; Riverside, California, M. Leitner; Las Vegas, Nevada, M. Kaneta; Alexandria, Virginia, L. Goldberg; Albuquerque, New Mexico, R. Nederhoff, S. Swetnam; Aurora, Colorado, M. Brown; Phoenix, Arizona, J. Martin, R. Turbow; Dallas,
Texas, J. Whitfield, T. Brannon; Roanoke, Virginia, R. Allen; Dayton, Ohio, N. Kantor, M. Belcastro; Ogden, Utah, N. Harper, J.
Berger; Columbia, South Carolina, S. Ellis; Panama City, Florida,
D. Sprague; Pensacola, Florida, A. Payne, J. Nagel; Reno, Nevada,
G. Yup; Tacoma, Washington, J. Mulligan, G. Jordan, R. Knudson;
Ponce, Puerto Rico, E. Ochoa, J. Rodriguez; Santurce, Puerto Rico,
F. Caceras; Barrington, Illinois, F. Uraizee; Fort Worth, Texas, M.
Stevener, R. Sidebottom, D. Turbeville, M. Stanley; Charleston,

990

West Virginia, S. Maxwell; San Juan, Puerto Rico, A. Rivera, M.

Ortega; Austin, Texas, J. Courtney, D. Wermer, J. Scharnberg; San
Jose, California, E. Alderete; Rock Hill, South Carolina, W. Helmuth; South Bend, Indiana, R. White; Kansas City, Missouri, S.
Shaffer, B. Heimes,; Pasadena, California, R. Liberman; Elmira,
New York, J. Felix, R. Sanders; Wichita, Kansas, B. Bloom; Ft
Lauderdale, Florida, E. Otero; Boca Raton, Florida, F. Miller, H.
Brenker; Coral Springs, Florida, J. Colindres; Fountain Valley,
California, V. Chundu; San Luis Obispo, California, S. VanScoy;
Laguna Hills, California, R. Naglie; Colorado Springs, Colorado,
D. Rommes, K. Meredith; Tucson, Arizona, C. Flores; El Paso,
Texas, L. Ayo, R. Caviglia, E. Ponte; Oklahoma City, Oklahoma, S.
Lopez, J. Pineda; Chattanooga, Tennessee, V. Thomas; Baltimore,
Maryland, H. Birenbaum, T. OBrien; Cheverly, Maryland, A.
Fomufod; Seattle, Washington, J. Prueitt, T. Sweeney, Yakima,
Washington, R. Skarin; Greenville, South Carolina, D. Wells, R.
Newell; Augusta, Georgia, A. Blalock; Melbourne, Florida, J. Vallette; St Louis, Missouri, J. Brenner, M. Maurer; Chesterfield, Missouri, W. Chao; and Mayaguez, Puerto Rico, E. Sanchez.

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Extrauterine Growth Restriction Remains a Serious Problem in Prematurely

Born Neonates
Reese H. Clark, Pam Thomas and Joyce Peabody
Pediatrics 2003;111;986
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http://pediatrics.aappublications.org/site/misc/reprints.xhtml

PEDIATRICS is the official journal of the American Academy of Pediatrics. A monthly

publication, it has been published continuously since 1948. PEDIATRICS is owned, published,
and trademarked by the American Academy of Pediatrics, 141 Northwest Point Boulevard, Elk
Grove Village, Illinois, 60007. Copyright 2003 by the American Academy of Pediatrics. All
rights reserved. Print ISSN: 0031-4005. Online ISSN: 1098-4275.

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