Abilities
of Children
Who
Were
Small-for-Gestational-Age
Babies
David
Harvey, FRCP, Joyce Prince, BA, Jim Bunton, BSc,Christine
Parkinson, MPhil, and Stuart Campbell, FRCOGFrom the Institute of Obstetrics and Gynaecology, Queen Charlotte ‘s Maternity Hospital, London
ABSTRACT. A follow-up study of 51
small-for-gesta-tional-age babies, whose intrauterine growth was moni-toned by serial ultrasonic cephalometry, was carried out at a mean age of 5.1 years. The developmental abilities of the children were assessed by using the McCarthy Scales of Children’s Abilities and the results were compared with those of a group of matched control subjects. Chil-dren whose head growth began to slow before 26 weeks’ gestation had significantly lower scores for the general cognitive index than control children. This did not occur
in children whose head growth began to slow later in
gestation. Scores for Perceptual-Performance and Motor scales in the McCarthy scales were also lower for the
children whose head growth slowed before 26 weeks’
gestation, when compared with those of control children. There were no differences in the developmental scores of the children when they were divided into groups accord-ing to birth-weight percentiles. We conclude that pro-longed slow growth in utero affects a child’s later devel-opment and abilities, in particular, perceptual perform-ance and motor ability. Pediatrics 69:296-300, 1982; small for gestation, ultrasonography, follow-up, brain growth, psychometry.
Babies who are small-for-gestational age (SGA)
at birth have more problems later than normal
children. They continue to grow slowly,’9 have an
increased incidence of mental handicap, and
edu-cational and behavioral problems.’4 However, it is
difficult to predict from birth weight alone which
SGA
babies will continue to be small or to haveproblems.38
A
previous report of an assessment at 4 years ofage of 60 SGA babies, born at term,7 showed that
Received for publication Jan 28, 1979; accepted June 19, 1981.
Reprint requests to (D.H.) Institute of Obstetrics and
Gynaecol-ogy, Queen Charlotte’s Maternity Hospital, Goldhawk Rd,
Lon-don, W6 OXG, England.
PEDIATRICS (ISSN 0031 4005). Copyright © 1982 by the American Academy of Pediatrics.
those children whose skull growth had begun to
slow in utero before 34 weeks’ gestation were more
likely
to be short and lower than average weight at 4 years. Children with onset of growth failure before26 weeks’ gestation also had significantly lower
development quotients by the Griffith’s extended
scales. Intrauterine head growth had been
meas-ured serially during pregnancy by ultrasonic
ceph-alometry.
We report a psychometric assessment of these
children and a comparison of their abilities with
those of a control group of children of normal birth weight.
METHODS
Subjects
Fifty-one children who were SGA at birth were
assessed at a mean age of 5.1 years, range 3 to 7
years (only two of the children were less than 3.9
years when tested). Their birth weights were below
the tenth percentile for gestational age after
allow-ing for maternal height and weight and the baby’s
sex’5; a further subdivision by birth weight showed
that 27 babies had a birth weight below the fifth
percentile for gestational age and the remainder (24
babies) had a birth weight between the fifth and
tenth percentiles. Each SGA child was matched
individually for sex, social class, birth order, and
birth
date (within six months) with a normal birth weight child.All babies were born in the hospital at 37 or more
completed weeks of gestation. The gestation was
measured by a careful history of the last menstrual
period. At the time the babies were born, serial
ultrasound was used only for selected patients; the
mothers were referred because of a clinical
suspi-cion for a small-for-date fetus. The babies had
resusci-rn
w
90
centiles 95th
50th 5th
70
c60
50
DII. 4Owks
14 16 20 22 24 26 28 30 32 3 36 38 40
Weeks Gestation
Fig 2. Ultrasound measurements of fetal head growth of child from group X, plotted on normal curves.
110-Cephalometry Chart
of a Group Y Child centiles -95th .50th .5th 100 - commencement of growth
retardation at 35 weeks
go-
8o-Q) E
36wks
40
.Q)
.9.40
03 E
E
C
0)
E
0) U
C
30
10
tation, early feeding, attention to temperature
con-trol, and the detection of hypoglycemia; there were
no serious neonatal illnesses and, in particular,
there were no babies with congenital anomalies,
symptomatic hypoglycemia, or congenital viral in-fection.
Permission for the study was obtained from the
hospital ethical committee and consent was also
obtained from the parents of each child to be tested.
Ultrasound Information
In the SGA group, serial measurements of the
biparietal diameter (BPD)’6 were begun before 30
weeks gestation and continued to within two weeks
of delivery.
The time of onset of slow head growth was
as-sessed by comparing BPD measurements with
nor-ma! BPD curves.’7 Slow growth was defined as
beginning when a weekly increment in the size of
the BPD fell below the fifth percentile over two
weeks or more, as described by Campbell and
New-man’7 and shown in Fig 1.
The SGA group was subdivided according to the
time of onset of slow growth in utero. In ten babies
this occurred before 26 weeks’ gestation and this
group has been named group X. Fig 2 shows the
cephalometry chart of one baby from group X,
plotted on the normal curves which give the fifth,
50th, and 95th pecentiles of the BPD against
ges-tation.
The remaining 41 SGA babies have been named
group Y; 23 showed growth failure at later stages of
pregnancy and 18 had no ultrasonic evidence of
intrauterine growth failure. In previous reports, we
subdivided this group into three but here the results
have been combined as group Y as they showed no
subgroup differences. Fig 3 shows a typical
cepha-lometry chart for a group Y baby who had growth
failure during the later stage of pregnancy.
50
::
-.--*
I I I I I I I I I
45 50 55 60 65 70 75 80 85 90 95 100
Biparietal diameter (mm)
Fig I. Normal curves used to relate biparietal diameter to weekly increment in its size. (Reproduced with per-mission from Campbell and Newman.’7)
Cephalometry
Chartof a Group X Child
______I I I I I I I I I I
14 16 18 a 22 24 26 28 30 32 34 36 38 40
Weeks Gestation
Fig 3. Ultrasound measurements of fetal head growth
of child from group Y, plotted on normal curves for
biparietal diameter.
Maternal history was reviewed for all groups but
no differences were found between them; in
partic-ular, there was no significant difference in the
TABLE 2. McCarthy Scale by Intrauterine Head Growth*
Scale Item Group X
(n = 10)
53.4 ± 11.4
51.5 ± 7.0
Group Y
(n=41)
56.7 ± 11.6
58.0 ± 10.9 P Value
NS
<.05
TABLE 1. McCarthy Scales for Infants With
Retar-dation of Intrauterine Head Growth Before 26 Weeks’
Gestation*
TABLE 3. McCarthy Scales for Infants With
Retar-dation of Intrauterine Head Growth After 26 Weeks’
Gestation*
Scale Item Group Y (n=41)
56.7 ± 11.6
58.0 ± 10.9
Control Sub-jects (n = 41)
57.5 ± 9.0
59.2 ± 10.7
* Values are means ± SD. Abbreviation used is: GCI,
general cognitive index.
P Value
NS NS
Birth weights were below the fifth percentile for
gestational age (mean birth weights: group X = 1.80
± 0.44 kg and group Y = 2.40 ± 0.29 kg) in 70% of
group X and 30% of group Y. The 51 control
chil-dren all had birth weights above the tenth percent-ile (mean birth weight = 3.36 ± 0.20).
Psychometry
All 102 children were assessed by means of the
McCarthy Scales of Children’s Abilities’8; those
giv-ing the tests (J.B. and J.P.) had no knowledge of
the groups the children were in. These scales were
chosen for this part of the study because they
provide data for specific abilities of children as well as their general abilities. Traditional intelligence
tests are limited
in this
respect; the Stanford-Binet gives only one standardized score for general abilityand the Wechsler Scales provide two subscores,
Verbal and Performance. The McCarthy subscores
include Verbal, Perceptual-Performance,
Quantita-tive, Memory, and Motor; the first three are
com-bined to give the general cognitive index (GCI). The
GCI
correlates significantly with the full-scaleWechsler and the Stanford-Binet scores.’8 For our
group of SGA children, we felt these scales would
be the most appropriate for determining the areas
in which they had most difficulties. The McCarthy
scales have limited use
in
Great Britain and theiris on American children. All results
we compared by using the Student t test.
differences between group Y children and the
con-trol subjects (Table 3).
When the results were compared by birth weight
alone, there were no significant differences in the
scores of children who had birth weights below the
fifth percentile, those with birth weight between
the fifth and tenth percentiles, and those with birth
weights greater than the tenth percentile (control
group).
Subscales
The results for testing of the subgroups on the
McCarthy Scales are also shown in Tables 1 to 3.
Group X children had significantly lower scores
than the control subjects for the
Perceptual-Per-formance scales and the Motor scales (P < .01)
(Table 1). Their scores were also lower than those
of group Y children (the other SGA group) on the
Perceptual-Performance (P < .05), Quantitative (P
< .02), and Motor (P < .05) subscales (Table 2).
There were no significant differences between
group Y children and the control subjects (Table
3).
A
comparison of the GCI of 37 of the SGAchil-dren with their developmental scores obtained a
year earlier with Griffith’s Scales showed a highly
significant correlation between the two
develop-mental tests (r = .65; P < .001), although a
com-parison between means showed that the McCarthy
scores (mean ± SD = 111.5 ± 15) were significantly
RESULTS
General Cognitive Index
A
comparison of group X children (those whoseintrauterine head growth slowed before 26 weeks’
gestation) with their ten control subjects showed
that they had significantly lower scores
(P
< .02)(Table 1). The results for group X children were
also significantly lower than those of group Y chil-dren
(P
< .05) (Table 2). There were no significantScale Item Group X
(n = 10)
Control
Sub-jects (n = 10)
P Value
Verbal 53.4 ± 11.4 59.8 ± 8.1 NS
Perceptual-Per- 51.5 ± 7.0 63.5 ± 8.1 <.01
formance
Quantitative 49.2 ± 6.6 54.0 ± 11.2 NS
Motor 45.1 ± 6.8 58.8 ± 11.2 <.01
Memory 46.8 ± 9.0 52.7 ± 10.9 NS
GCI
102.9±
11.7
118.0±
12.9
<.02
Verbal
Perceptual-Per-formance
Quantitative 49.2 ±
6.6
55.7
± 8.4 <.02Motor 45.1 ± 6.8 51.1 ± 11.3 <.05
Memory 46.8 ± 9.0 52.2 ± 9.7 NS
GCI 102.9 ± 11.7 113.2 ± 16.4 <.05
* Values are means ± SD.
Verbal
Perceptual-Per-formance
Quantitative 55.7 ± 8.4 56.7 ± 10.0 NS
Motor 51.1 ± 11.3 53.3 ± 8.9 NS
Memory 52.2 ± 9.7 56.9 ± 9.1 NS
GCI 113.2 ± 16.4 115.0 ± 15.2 NS
higher than the Griffith’s scores (mean ± SD = 102.3 ± 12)
(P
< .01).DISCUSSION
This study shows poor performance of children
who were SGA at birth and who had slow head
growth
in
utero starting before 26 weeks andcon-tinuing until near term (group X). They form part
of a group of children who do not grow well in
childhood,7”3 unlike SGA babies with normal head
growth in utero who rapidly catch up after birth.’9
Previous studies have shown many of the problems
that SGA babies are likely to have: poor school
performance, lower intelligence, behavior problems, and other handicaps.’’4
The McCarthy Scales of Children’s Abilities were
used to determine the specific problems of group X
children. The study has shown that they had lower
scores for the GCI than the control subjects, and a
major contribution to this was their lower
Percep-tual-Performance subscores. This subscore
mea-sures a child’s ability to understand and carry out
instructions, and to copy and classify given shapes.
In another study of these children, which involved
a detailed neurologic assessment,#{176} group X children
had difficulties in copying matchstick shapes, which confirms that they have perceptual problems.
This study has also shown that the group X
children did less well on the Motor subscales of the
McCarthy Scales. A neurologic assessment of the
same children confirmed that they have difficulty
with tests of coordination and balance.2#{176}
A
schoolteacher’s assessment of group X childrenshowed that they have particular problems with
reading and writing, especially the boys, who were
also thought to be clumsy.’4
These results give further evidence that it is
possible to predict at birth, on the basis of
intra-uterine ultrasonic growth pattern alone, which SGA
babies are most likely to have later problems. We
have been able to confirm the work of Fitzhardinge and Steven” that birth weight itself is not the best
indicator of an infant’s later growth and
develop-ment. Ultrasonic cephalometry is now a standard
method of measuring the growth of the fetus in
utero. This technique probably reveals particularly
severe growth failure because brain growth is
thought to be less affected than the growth of other
organs in the malnourished fetus.2’
It is not possible to determine what has caused
the poorer developmental scores in the children
whose slow intrauterine growth began before 26
weeks’ gestation, but it may be related to growth
retardation occurring during vital periods of brain
development.
Animal studies have shown that growth
restric-tion in utero results in a reduction in brain size,
which affects the weight of the forebrain and of the cerebellum.2225
The pattern of human fetal and neonatal brain
growth has been demonstrated by Dobbing and
Sands.26 There is a period of rapid growth of the
whole brain from midgestation to 2 years of
post-natal age. Neuronal multiplication in the forebrain
occurs between 10 to 18 weeks’ gestation and is
immediately followed by multiplication of the glial
cells. It is therefore possible that retardation of
brain growth
in
the second trimester of pregnancymay affect both cerebral and cerebellar
develop-ment; the cerebellum may be more vulnerable to
growth retardation because it has a rapid growth
rate.
Our results for the GCI confirmed previous
find-ings, by using the Griffith’s scales, that group X
children had lower scores. As our control subjects
were carefully matched, it is unlikely that the lower
scores in group X children were caused by
environ-mental factors. It is interesting that the McCarthy Scales gave higher scores than the Griffith’s Scales, although there was a highly significant correlation
between the two tests. It is possible that the
Mc-Carthy tests give the child more opportunity to
display a variety of skifis, since it tests a wider range of ability. Alternatively, the Griffith’s test has been
standardized on English children and this has not
yet been carried out for the McCarthy Scales.
These results show that ultrasonic studies of fetal
growth provide a good guide to the prognosis for
SGA babies. It is, therefore, useful to perform an
ultrasound examination at around 16 weeks’
gesta-tion to provide accurate dating and a base line for
fetal growth.
ACKNOWLEDGMENTS
This work was supported by a grant from a trust.
We thank Dr Robyn Fancourt for her work in the
initial follow-up study of these small-for-gestational-age babies, and Dr Sheila Wallis for her work in subsequent follow-up studies and for finding the control subjects.
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17. Campbell S, Newman GB: Growth of the fetal biparietal
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18. McCarthy D: Manualfor the McCarthy Scales of Children’s Abilities. New York, The Psychological Corporation, 1972
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20. Waths S, Shamsi D, Harvey D: Neurological examination of
children who were small-for-dates babies, in Salvadori B, Bacchi Modena A (eds): Poor Intrauterine Fetal Growth. Rome, Centro Minerva Medica, 1977, P 567
21. Gruenwald P: Chronic fetal distress and placental insuffi-ciency. Biol Neonate 5:215, 1963
22. Dobbing J, Hopewell JW, Lynch A: Vulnerability of devel-oping brain. VII. Permanent deficit of neurons in cerebral
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23. Culley WJ, Lineberger RD: Effect of undernutrition on the
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25. Bourre JM, Morand 0, Chanez C, et al: Influence of
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WAS MATTHEW ARNOLD’S CROOKED LEG CAUSED BY RICKETS?
Matthew Arnold (1822-1888), poet and critic, the second child (of nine) and
oldest son of Thomas and Mary Arnold, had a crooked leg and spent two years
of his childhood in heavy iron braces-the family nicknamed him “Crabby” for
his shuffling gait.
Park Homan1 in his recently published biography of Matthew Arnold
de-scribes the treatment Arnold received for his crooked leg as follows:
Instructing his infants in oarsmanship, the father now took them out on the Trent in the Frolic. . . .Within a day or two of this time, she [Mrs. Arnold] noticed that something was wrong with Matthew’s leg. . .. But within ten days of leaving the River Trent, the
Arnolds consulted Mr. Tothill, back at home, and then a London specialist-with the
result that a frightening iron apparatus arrived .. . to be fitted to his limbs. His father
was not deeply worried: ‘We have had some anxiety about Matt,’ Thomas Arnold wrote
to a friend . .. ‘from the Effects )f a bad habit of crawling before he could walk, and which was greatly bent one of his Legs, so that he has obliged to wear Irons, and must
continue to do so for some time.’
At two or three, most children become excitedly aware of themselves in relation to other people, but Matthew found that thick leg-straps and leg-braces of the heaviest iron made him peculiar and decidedly ugly. He found it difficult to move about and reacted very audibly. ‘I also remember,’ he writes at 13, ‘wearing irons and being obstinate and
being taken up to London about my crooked legs.’ Mrs. Arnold understood her little
boy’s obstinancy and tears. Pediatricians who have examined her comments believe that rickets had increased bowing of the tibia in her young child; the weight of cast-iron braces
soon bent his one good leg. She took him up to town to plead with an orthopedic
specialist-but Dr. Carpus was invisible on one occasion and quite adamant on another. Beside herself with worry, she thought of defying Dr. Carpus’s explicit orders-and wavered.
REFERENCE
Noted by T.E.C., Jr, MD