(Received May 22; revisions accepted for publication October 10, 1969.)
Supported in part by U.S. Public Health Service Grant HD-00351 and the Deutsche Forschungs.
gemeinschaft, Schu 120/11-14.
ADDRESS: (F.J.S.) Universit#{228}ts-Kinderklinik, University of C#{246}ttingen, Gothngen, West Germany.
ADDRESS FOR REPRINTS: (A.H.P.) UCLA Center for the Health Sciences, Los Angeles, California 90024.
PEDIATRICS, Vol. 45, No. 1, Part I, January 1970
DEVELOPMENTAL
TESTING
OF
PRE-TERM
AND
SMALL-FOR-DATE
INFANTS
Arthur H. Parmelee, Jr., M.D., and Franz J. Schulte, M.D. Department of Pediatrics, UCLA Center for the Health Sciences, Los Angeles and
f/se Universit#{228}ts Kinderklinik, University of G#{246}ttingen, West Germany
ABSTRACT. Twenty-five full-term, newborn
in-fants and 22 small-for-date infants born at term
had comparable nerve conduction velocities and
were considered to be of equal neurological
matur-ity. Twenty-six pre-term infants e(Iual in weight to
the small-for-date infants had significantly slower
nerve conduction velocities and were considered on
this basis more immature at birth than the term
and small-for-date infants. All of these infants were given Gesell developmental tests at approxi-mately 40 weeks of age by an examiner with no
knowledge of their neonatal condition. The
objec-tive was to determine to what degree performance
later in infancy is dependent on neurological
ma-turity at birth.
The full-term infants and the small-for-date
infants performed at their age level with average developmental qusotients of 99 and 96,
respec-tively. The pre-term infants performed at less than
their age from birth with an average D.Q. of
88; but, when their age was corrected for weeks
of prematurity, the average D.Q. was 99. These
findings substantiate the concept that performance
on the Cesell schedules is dependent on time from
conception rather than time from birth. Pre-term
infants shousld have their age determined from
their expected date of birth for purposes of
cal-culating a developmental quotient. Pediatrics,
45:21, 1970, DEVELOPMENTAL TESTING, PRE-TERM
INFANTS, SMALL-FOR-DATE INFANTS, NERVE
CONI)UC-TION VELOCITY, NEUROLOGICAL MATURATION,
NEWBORN INFANTS.
N
EWBORN infants are no longer judgedas pre-term only on the basis of a
birth weight of 2,500 gm or less. It is now
recognized that infants can be born at term
with birth weights far less than 2,500 gm.
The name “small-for-date” has been used to
include both term and pre-term infants
with birth weights below the 10th
percen-tile for their gestational age.1’2 These
judg-ments have been made possible by the
pub-lication of birth measurement tables for
various gestational ages.3-5
The neurological maturity of three
groups of infants-pre-term, “small-for-date”
at term, and term controls-was established
by the nerve conduction velocity
measure-ments reported in a previous paper.6 This
second study presented the opportunity to
observe if neurological maturity was still a significant factor in behavioral development
in the last quarter of the first year of life.
The three groups of infants studied in
the neonatal period6 were given the Gesell
Developmental test at 9 months to 1 year
from their expected date of delivery. The
level of developmental performance was
then compared with their actual age from
time of birth to determine to what degree
neurological maturity at the time of birth
contributed to later performance. If degree
of neurological maturity at birth were not a
significant factor, then developmental level
would be a function of actual age from
birth. On the other hand, if neurological
maturity at birth were important, then
de-velopmental level would be a function of
the time from the expected date of birth.
That is, developmental level in all cases
would be a function of age from
Infant
GestationBirth Weight
(wk) (gm)
Mean S.D. Mean S.D.
25 39.6 0.8 3479 323
26 3.5.2 1.5 2301 325
20 i 39.4 1.6 2169 266
Birth Length
(cm)
Birth IIcad
Circumference (cm)
Mean S.D. Mean S.D.
54 1.7 33.1 0.9
47 2.2 32.1 1.7
47 1.8 ‘32.6 1.2
SUBJECTS AND METHOD
Three groups of infants were studied:
full-term controls, pre-term infants, and
small-for-date infants. The full-term control
infants, all born in the Obstetrical
Depart-ment of the University of GOttingen, were
carefully selected as having a history of
normal gestation, labor, delivery, and
neo-natal adjustment and were of normal size
(Table I). They were also normal on
neu-rological examinations done 3 to 8 days
after birth.
The pre-term infants were selected to
match the small-for-date term infants as a
group on weight (Table I). These infants
were all from the nursery of the Children’s
Hospital of the University of Gottingen, and
all had weights between the 10th and 90th
percentile for their gestational ages.
In-cluded in this group were six sets of twins
and one set of triplets. All of the pre-term
infants were neurologically normal, except
one who had a hemisyndrome.
The small-for-date babies were all
re-ported by their mothers to be of more than
37 weeks’ gestational age at birth. They
were all from the nursery of the Children’s
Hospital of the University of Gottingen.
Those infants in which there was
consider-able doubt about the gestational period
be-cause of irregularities of the mother’s
menses or inadequate gestational histories
were not included in this study. Included
were two sets of twins. These babies were
all below the 10th percentile on both the
Hosemann and ‘ intra-uterine
growth charts. Seven of these l)ahies had
deviant neonatal neurological findings. Two
had a single syndrome : hyperexcitability
and hypotonia. Five had combinations of
syndromes, such as apathy, hypotonia, and
hemisyndrome. No small-for-date infants
were included who had a recognizable
chroniosomal defect, such as mongolism, or
an obvious congenital anomaly. Blood
sug-ars were measured in all of the
small-for-date infants and were found to be below 30
mg! 100 ml on at least two occasions in six
babies; five of these infants had neonatal
neurological findings or symptoms.
Infants with neonatal neurological signs
were included in the original study6 to
de-termine whether or not nerve conduction
was independent of these neurological
find-ings, and this proved to be true. With three
exceptions to be described, they were
therefore, kept in the follow-up study
be-cause our sample size was small. Moreover,
the possibility that they might have lower
D.Q. scores because of a neurological
prob-lem, in any case, would work against our
contention that development is a function
of post-conception age, as would be
re-flected in the similarity of the
small-for-date and the full term infants’
developmen-tal ages. The several sets of twins,
espe-cially among the pre-terms, and the triplets
were intentionally included in the neonatal
nerve conduction study since they served as
their own controls because they were of
identical gestational ages but differed in
TABLE I
Normal control Pre-term Small-for-date
Number of
Infanl.c
ARTICLES 23
Full
-term
Controls
n
25
+8wks. +4wks.
/
/
/
/
/
/
/
(1
a)
a)
E
0.
0 a)
> a)
0
54
50
46
42
38
34
-4wks.
/
x/
X//
/
/
/
,-8wks.
/
/
/
/
/
/
/
DQ:99±
8.6
38
42
46
50
54
SAge From
Birth
(wks.)
FIG. 1. Plot of each full-term infant’s development age score on the Gesell
test against his chronological age from birth. Broken lines indicate where
scores 4 and 8 weeks greater or less than age from birth would fall and solid line where scores equal to chronological age would fall. Average D.Q. = 99;
standard deviation = 8.6.
birth weight. The neurological examination
technique and the definition of the neonatal
neurological syndromes have been
pre-viously published, as have the techniques
and results of measuring nerve conduction
times in newborn infants 5i,S
There were four term, three pre-term,
and two small-for-date infants who did not
return for a developmental examination or
could not be located. Twenty-five full-term
controls, 26 pre-terms, and 22 small-for-date
infants were successfully re-examined.
The appointments for the follow-up
ex-amination were planned for each infant
when he was 9 to 10 months of age (39 to
44 weeks) as calculated from the mother’s
expected date of confinement (EDC). In
the case of the term and small-for-date
in-fants, this coincided with their age from
birth. For the pre-term infants this age was
less than their age from birth by the
num-ber of weeks of prematurity. No subjects
were less than 36 weeks or more than 52
weeks from EDC.
Gesell developmental examinations were
given by an examiner (A.H.P.) who had
not seen the infants in the neonatal period
and did not know which group the infant
was in. The only information the examiner
had was the infant’s age calculated from
the EDC. This was done to equate the con-ceptional ages of the term and pre-term in-fants.
The Gesell test was scored by giving a
developmental age for five categories of
performance: gross motor, fine motor,
adap-tive, language, and social. The total score
was the average of these subscores. This
varies from the Gesell schedules only in
+8wks. +4wks. ,
/
//
/
/
/
54
50
46
42
38
34
-4wks.
/
/
/
/
/
/
/
/
x
/
x
. -8wks.
/
/X
8.8
50
54
DQ :96±
x
38
Age
From
Birth
(wks.)
were scored separately as fine motor, and
the remaining motor items were scored as
gross motor.
Three children who had been included
in the original neonatal study6 and returned
for developmental assessment could not be
satisfactorily examined and were, therefore,
excluded from the neonatal and follow-up
data. One small-for-date infant came for
Gesell testing twice but was so irritable and
apprehensive that no test could be done.
He had had apathy, hypertonia,
hemisyn-drome, brief coma, and convulsions in the
neonatal period. Another small-for-date
baby had apathy, hypotonia,
hemisyn-drome, and convulsions in the neonatal
pe-riod. He was grossly retarded at 52 weeks
of age; his estimated D.Q. was 25. Similarly
there was one pre-term baby with neonatal
coma and convulsions who at 46 weeks of
age had severe cerebral palsy and had an
estimated D.Q. of 30.
RESU LTS
The 25 control term infants had a mean
D.Q. of 99 and s.d. = 8.6. Their
develop-mental ages were all close to their age from
birth, with no major deviations (Fig. 1).
Four had D.Q.’s below 90 and none below
80.
The 22 small-for-date infants born at
term had a mean D.Q. of 96 and s.d. = 8.8.
Their developmental ages were also close to
their ages from birth, with a few major
ex-ceptions (Fig. 2). Five had D.Q.’s below 90
and one of these was below 80.
The 26 pre-term infants had a mean D.Q.
of 88 and s.d. = 9.1 based on their ages
from birth not corrected for weeks of
pre-maturity. Except for one set of twins, their
a)
0
C
a)
E
0.0
a)
> ci) 0
Small
-for
-Dates
n =
20
Fic. 2. Plot of each small-for-date infant’s developmental age score on the
Cesell test against his chronological age from birth. Broken lines indicate
where scores 4 and 8 weeks greater or less than age from birth would fall
and solid line where scores equal to chronological age would fall. Average
ARTICLES
Pre
-terms
n
26
25
+8wks. +4wks.
/ /
/ /
/ x/
/
/
/
/
/
/
50
46
/
/4wk5.
/
/
ui
-a)
0
C
a)
E
0.
0
a)
0)
0
/
/
/
/
/
,-8wks.
/
42
/
/
/
/
/
/
X/ x,
/
38-/
x
34.
00:88± 9.1
38
42
46
Age
From
Birth
(wks.)
FIG. 3. Plot of each pre-term infant’s developmental age score on the Cesell test against his chronological age from birth. Broken lines indicate where
scores 4 and 8 weeks greater or less than age from birth would fall and solid
line where scores equal to chronological age would fall. Average D.Q. = 88;
standard deviation = 9.1.
developmental ages were all below their
ages from birth. Sixteen D.Q.’s were below
90, and six of these were below 80 (Fig. 3).
However, the pre-term infants had a mean
D.Q. of 99 and s.d. = 9.4 when based on
their corrected ages, i.e., age from EDC,
with their developmental ages
correspond-ing more closely to their corrected ages
with a few exceptions (Fig. 4). Five had
corrected D.Q.’s below 90 and none of
these were below 80.
Among the 22 small-for-date infants, the
seven who had deviant neonatal
neurologi-cal findings did not have D.Q. scores that
were significantly different than the others,
or the full-term controls.
DISCUSSION
Our findings substantiate the concept
that performance on the Gesell schedules is
dependent on time from conception rather
than time from birth. Pre-term infants
should have their age calculated from the
expected date of birth for purposes of
cal-culating a developmental quotient.7 As the
child becomes older, this correction factor
becomes proportionately smaller compared
with the total age. It is most significant in
the first years of life.
The small-for-date infants performed at
or near their age from birth on follow-up
testing. Thus, provided that these infants
are not neurologically abnormal at birth
and only have transient neonatal findings
and have no major physical defects, their
further development during the first 9
months need not be jeopardized by the low
birth weight itself. At 9 months the
small-for-date infants’ mean D.Q. was not
con-+8wks. +4wks.
/ /
/
54
50
46
/
X/
/
/ /
/
,-4wks.
/ /
U
ci)
0
C ci)
E 0. 0 a)
>
a)
0
/
,-8wks.
/
x
xx
42
/
38
/
/
x /
/
/
/
/
/
/ x//
/38 42 46
50
54
58
34.
/
/X
/XX
/
/ X/
/X /
/
DQ:99±9.4
Pre
-terms
n: 26
Age
From
E. D. C. (wks.)
FIG. 4. Plot of each pre-term infant’s developmental age score on the Gesell test against his corrected age, i.e., age from I)irth minus number of weeks of prematunty. Broken lines indicate where scores 4 and 8 weeks greater or less than corrected age would fall and solid line where scores equal to corrected
age would fall. Average D.Q. = 99; standard deviation = 9.4.
trols or pre-term infants whose ages were
corrected for degree of prematurity.
The pre-term infants were similar to the
full-term controls with respect to mean
D.Q.’s and number of D.Q.’s below 90. It
has been reported that pre-term infants do
not do as well on Gesell developmental
ex-aminations at 9 months of age as full-term
infants, but this was primarily due to the
inclusion of babies of very low gestational
ages and birth weights. In our study the
pre-term infants averaged 35 weeks’
gesta-tional age and 2,301 gm. birth weight. It
should be remembered that these pre-term
infants were originally selected to match
the term small-for-date infants in weight. It
is known that the incidence of retardation
is greater in very premature infants.’
We realize the importance of
environ-mental factors in determining the
develop-mental performance of babies within the
first year of life. It was well-known to
Ge-sell that babies who receive inadequate
stimulation can be delayed in their
development. At the time of our
develop-mental examination, questions were asked
concerning the amount and type of
parent-child interaction to check on this point. No
gross family inadequacies were found.
Therefore, we feel that the developmental
performances of the babies we studied
were largely a function of their
neurologi-cal maturation from conception.
Measures of degree of physical and
neu-rological maturity for each gestational age
have been sought that are independent of
birth weight. Clinical criteria (such as skin
color, opacity, and texture) have been
cor-related with gestational age)2 The normal
ARTICLES 27
despite lags in other measurements, in
small-for-date infants has been 3’ 14
The brain appears to be spared to a major
degree. Clinical neurological &3
and electroencephalographic 7 2 I
have been developed for maturation and
gestational age, which also indicates that
brain maturation continues despite lags in
weight and height. However, these clinical
and EEG criteria may be altered by acute
perinatal problenis (such as hypoxia,
dehy-dration, or infection ) so that the maturity
of an infant in distress may be difficult to
judge. Nerve conduction velocity is a more
satisfactory criterion of neurological
matu-ration since it is less vulnerable to
distor-tion when acute perinatal disturbances are
present.25 Small-for-date infants born at
term have velocities comparable to those of
a group of infants of normal birth weight
born at term, whereas pre-term infants
matched on weight with the small-for-date
infants have significantly longer conduction
velocities.’
Several of the previously cited studies
have indicated that neurological maturation
is not observably accelerated or delayed by
extra-uterine life in the case of pre-term
birth.19’2#{176}That is, the infants born pre-term
were similar in their neurological responses
at their expected date of delivery to infants
born at term. The present findings also
in-dicate the importance of considering the
neurological maturity of the infant at birth
in evaluating his subsequent development.
IMPLICATIONS
The implications of this study are that
neurological maturation is a dominant
de-terminant of behavioral development as
measured by the Gesell schedules in the
first year of life. The factors provided by
earlier extra-uterine existence in the case of
immature pre-term infants do not advance
and apparently need not retard behavioral
development. This implies that, as long as
an adequate level of environmental
stimula-tion is provided, development proceeds
nor-mally. It does not negate the possibility
that extra environmental stimulation might
not advance behavior, particularly some
be-haviors no tested in this situation. It does,
however, re-emphasize the very real
limita-tions imposed by immaturity of the nervous
svsteni upon the rate of development.
SUMMARY
A previous study demonstrated that a
group of full-term infants and a group of
small-for-date infants born at term had
sim-ilar nerve conduction velocities. They were
therefore equal in neurological maturity on
this measure. On the other hand, a group of
pre-term infants matched as a group in
weight with the small-for-date infants had
nerve conduction velocities that were
sig-nificantly slower. They were, therefore,
neurologically more immature by this
mea-sure. Seven of the small-for-date and one of
the pre-term infants presented deviant
neo-natal neurological findings which did not
alter their nerve conduction times and were
apparently transient.
All three groups of infants, 25 full term,
22 small-for-date, and 26 pre-term, were
given a Gesell Developmental test at 40
weeks of age by an examiner who was
un-aware of their neonatal condition. The level
of developmental performance was then
compared with their actual age from time
of birth to determine to what degree
neuro-logical maturity at the time of birth
con-tributed to later performance.
The full-term infants and the
small-for-date infants all performed at or near their
chronological age level with average
Devel-opmental Quotients of 99 and 96,
respec-tively. The pre-ternl infants performed at
less than their chronological age, with an
average D.Q. of 88, but at or near their age
when a correction was made for the weeks
of prematurity, with an average D.Q. of 99.
The seven small-for-date and one pre-term
infant with deviant neonatal neurological
findings did not have D.Q. significantly
dif-ferent than the others.
These results substantiate the concept
that performance on the Gesell schedules is
dependent on time from conception rather
should have their age calculated from the expected date of birth for purposes of
as-signing developmental quotients.
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