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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, FRCOG

From 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 have

problems.38

A

previous report of an assessment at 4 years of

age 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 before

26 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

(2)

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

Chart

of 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

(3)

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 ability

and 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-scale

Wechsler 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 their

is 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 SGA

chil-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 whose

intrauterine 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 significant

Scale 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 <.02

Motor 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

(4)

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 and

con-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 children

showed 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 pregnancy

may 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.

REFERENCES

1. Usher RH, McLean FH: Normal fetal growth and the signif-icance of fetal growth retardation, in Davis JA, Dobbing J (eds): Scientific Foundations of Paediatrics. London, W.

Heinemann, 1974, p 69

2. Bard H: Intrauterine growth retardation. Clin Obstet Gyne-col 13:3, 511, 1970

3. Fitzhardinge PM, Steven DE: The small-for-date infant. I. Later growth patterns. Pediatrics 49:671, 1972

4. Neligan GA, Prudham D, Steiner H: The Formative Years. London, Oxford University Press, 1974

5. Van den Berg BJ, Yerushalmy J: The relationship of the

rate of intrauterine growth of infants of low birth weight to mortality, morbidity and congenital anomalies. J Pediat 69:

531, 1966

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birth weight. Acta Paediatr Scand 64:33, 1975

7. Fancourt R, Campbell 5, Harvey D, et al: Follow-up of small-for-dates babies. Br Med J 1:1435, 1976

8. Neligan GA, Kolvin I, Scott D, et al: Born too Soon or Born too Small. London, W Heinemann, 1976

9. Davies DP: Growth of ‘small-for-dates’ babies. Early Hum Dev 5:95, 1981

10. Bjerre I, Hanson E: Psychomotor development and school adjustment of seven year old children with low birth weight.

Acta Paediatr Scand 65:88, 1976

11. Fitzhardinge PM, Steven EM: The small-for-dates infant. II. Neurological and intellectual sequelae. Pediatrics 50:50,

1972

12. Francis-Williams J, Davies PA: Very low birth weight and

later intelligence. Dev Med Child Neurol 16:709, 1974

13. Wallis SM, Harvey DR: Small-for-dates babies, their prob-lems and their future, in: Wharton BA (ed): Topics in Perinatal Medicine. London, Pitman Medical, 1980 14. Parkinson CE, Wallis 5, Harvey D: School achievement and

behaviour of children who were small-for-dates at birth. Dev Med Child Neurol 23:41, 1981

15. Tanner JM, Thomson AM: Standards for birth weight at gestational periods from 32 to 42 weeks, allowing for mater-nal height and weight. Arch Dis Child 45:566, 1970 16. Campbell S: An improved method of fetal cephalometry by

ultrasound. J Obstet Gynaecol Br Commonw 75:586, 1968

17. Campbell S, Newman GB: Growth of the fetal biparietal

diameter during normal pregnancy. J Obstet Gynaecol Br Commonw 513:78, 1971

18. McCarthy D: Manualfor the McCarthy Scales of Children’s Abilities. New York, The Psychological Corporation, 1972

19. Brandt I: Growth dynamics of low-birth-weight infants with emphasis on the perinatal period, in Falkner F, Tanner JM (eds): Human Growth. London, Balliere Tindall 1978, vol 2,

P 557

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

and cerebellar cortex following early mild under-nutrition.

Exp Neurol 32:439, 1971

23. Culley WJ, Lineberger RD: Effect of undernutrition on the

size and composition of the rat brain. J Nutr 96:375, 1968 24. Cragg BG: The development of cortical synapses during

starvation in the rat. Brain 95:143, 1972

25. Bourre JM, Morand 0, Chanez C, et al: Influence of

intra-uterine malnutrition on brain development: Alteration of

myelination. Biol Neonate 39:96, 1981

26. Dobbing J, Sands J: Quantitative growth and development

of human brain. Arch Dis Child 48:757, 1973

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

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1982;69;296

Pediatrics

David Harvey, Joyce Prince, Jim Bunton, Christine Parkinson and Stuart Campbell

Abilities of Children Who Were Small-for-Gestational-Age Babies

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1982;69;296

Pediatrics

David Harvey, Joyce Prince, Jim Bunton, Christine Parkinson and Stuart Campbell

Abilities of Children Who Were Small-for-Gestational-Age Babies

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