Pediatric Exercise Science, 1998, 10, 327-336
0 1998 Human Kinetics Publishers, inc.
-
Muscle Function of 11 to 17-Year-Old Children
of Extremely Low Birthweight
Eric Small, Oded Bar-Or, Edgar Van Mil, and Saroj Saigal
This study compared the anaerobic performance and the muscle strength between extremely low birthweight (< 1,000 g = ELBW) 11- to 17-year-old
adolescents and normal birthweight (> 2,500 g = NBW) controls. Seventeen
ELBW (9 females and 8 males) and 17 NBW (9 females and 8 males) subjects
took part. ELBW had lower anaerobic performance, as manifested in mean (p
= .03) and peak ( p < .001) mechanical power per kg body mass (Wingate
Anaerobic Test). In absolute units mean power and peak power tended (p =
.06 and .08, respectively) to be lower in the ELBW group, but there were no
inter-group differences in the isokinetic strength of knee extensors or flexors
(Kin Com dynamometer). ANOVA revealed no interaction between the effects of low birthweight and gender. We propose that dynamic, but not static,
muscle performance in ELBW is still somewhat inferior in adolescence. This
may reflect deficient neuromuscular control.
Over the past decade, the survival rate of extremely low birthweight (ELBW)
infants (< 1000 g) has increased dramatically (9, lo), with a growing number of these
infants reaching teenage. Several studies have examined the neuromotor and neurosensory development of these children (28-30,35). Impairments have been shown in
behavior (22,29) and in social and cognitive skills (29,30). ELBW preschoolers are
often smaller in stature, compared to normal birthweight (NBW) children (17). In
addition, ELBW children have shown poor school performance (11, 12,28), motor
skill impairments (5, 18, 19,21,25), and lower motor proficiency (30).
There is no published information regarding the habitual physical activity and
24-hour energy expenditure of ELBW children and only a paucity of data regarding
their static muscle strength. In one study (8) static handgrip was found weaker among
5-year-old very low birthweight (VLBW < 1,500 g) children, even when corrected
for body mass. In contrast, aerobic fitness (measured as peak 0, uptake per kg body
weight) of 7- to 11-year-oldchildren with a VLBW was comparable to that of NBW
children (3). Arecent study has shown that anaerobic muscle power, using the Wingate
test, and neuromotor coordination components are deficient among ELBW 5- to 8year-old Israeli children (7). Low neuromotor coordination, as assessed by reaction
time, maximal cycling speed, and a whole-body coordination test, was also shown
E. Small, 0. Bar-Or and E. Van Mil are with the Children's Exercise and Nutrition
Center at McMaster University, Hamilton, Ontario, L8N 325,Canada. S. Saigal is with the
Neonatology Unit at McMaster University.
among ELBW 5- to 7-year-old Canadian children (15).
The above studies have focused, almost exclusively, on ELBW children at
the first decade of life. It is unknown, though, whether such sequelae of low
birthweight carry over to adolescence, or whether there is a catch-up in performance as the ELBW child goes through the second decade of life.
The purpose of this study was two fold: (a) to compare the anaerobic muscle
performance of the lower limb and the muscle strength of knee flexors and extensors
between ELBW adolescents and age- and gender-matched NBW controls; and (b) to
determine whether intergroup differencesin muscle performance can be explainedby
lean limb volume or by the level of physical activity. A secondary objective was to
find out whether the differences in muscle performance between the two birthweight
groups are gender related. We hypothesized that adolescents of ELBW, even when
they have no overt clinical manifestations of a neuromuscular disease, would have
deficient muscle performance compared with NBW controls.
Subjects and Methods
Seventeen ELBW (9 girls and 8 boys) and 17 NBW (9 girls and 8 boys), 11- to 17years-old, were recruited. The ELBW survivors are part of a regional cohort of
births, 500 to 999 g birthweight, born between 1977 and 1982 and followed longitudinally regarding intellectual and psychological functioning at the Children's
Hospital of the Hamilton Health Science Corporation (28-30). The controls in the
above longitudinal study had a normal birthweight (> 2,500 g) and were recruited
at age 8 years. Although these controls were not selected randomly from the general population, they were matched with the ELBW cohort for age, gender, and
socioeconomic status.
Groups for the present study were formed by selecting pairs of subjects from
the above two cohorts, then matching them for age and gender. Excluded were
those candidates with any overt disability or chronic medical condition such as
cerebral palsy or seizures. The university's Ethics Review Board approved the
study. Informed consent was obtained from a parent following the verbal assent of
the child. The subject characteristics are shown in Table 1. Both groups, when
subdivided by gender, were similar in terms of weight, percent body fat, sum of
skin folds, lean thigh volume, and Tanner stage. ELBW girls were significantly
shorter than NBW girls, while the height of the boys was similar in both groups.
Among the ELBW group, average duration of respiratory support was 36.5
days for the males and 30.4 days for the females. Average total number of days on
supplementaryoxygen was 50 days for the males and 41.9 days for the females. Four
of the males were small for gestational age (SGA), and 4 were appropriate for gestatioGal age (AGA). The respective numbers for the girls were 2 SGA and 7 AGA.
Bronchopulmonary dysplasia (BPD) was diagnosed in 4 males and 3 females.
Measurements
Anthropometry
Body height was taken (Harpenden stadiometer, 0.1 cm resolution) with the barefoot child standing erect and inhaling fully. Body mass (Mott electronic scale,
accuracy 20 g), was measured of the barefoot child wearing t-shirt and shorts.
-
Table 1 Subjects' Physical Characteristics
Male
Variables
NBW
ELBW
Female
Significance
NBW
ELBW
Significance
Age (yr)
Height (cm)
Weight (kg)
Sum of skinfolds (mrn)
% Body fat
Lean thigh volume (L)
Tanner stage
Birth weight (g)
Gestational age (weeks)
+
Note. All values are expressed as M SD. NBW = normal birthweight. ELBW = extremely low birthweight. NS = no significance. Significance is
defined as p < .05.
3
P
3
330 - Small et a/.
Percentage body fat was assessed using a Valhalla bio-impedance machine with
the child in supine position. Skinfolds were taken in triplicate (biceps, triceps,
subscapular, suprailiac, anterior and posterior thigh, and medial and lateral calf),
and median value taken for further analysis. Lean thigh volume was calculated by
measuring thigh length, thigh circumference,and skinfold thickness at medial thigh
(13, 14).
Spirometer
Forced vital capacity (FVC) and forced expiratory volume in the first second (FEV,)
were determined in the upright position (Vitalograph spirometer). The best of three
attempts was used for statistical analysis.
Muscle Strength, Peak Power, and Endurance
Isokinetic knee flexion and extension strength of the right leg was measured, with
the subject in the sitting position, using a Kin Com isokinetic dynamometer. Angular velocity was 60" per second, at an angle of 90-20" relative to full extension.
Three sets of knee extension-flexion cycles were performed with 30-s rest interval
between trials. The highest value was then used for further analysis.
Peak power and muscle endurance were measured by the Wingate Anaerobic Test (1). This 30-s cycling test measures anaerobic performance. The test is
feasible for performance by healthy children and adolescents and those with a
physical disability (23, 32, 33) and is highly reliable in these groups (1, 6, 32). A
Fleisch-Metabo (Switzerland) mechanical ergometer was used, connected on-line
to a PC for data analysis and display of the results. Indices of performance included peak power (PP), which is the highest mechanical power (W) at any 3-s
period of cycling, and mean power (MP), which is the average power over the
entire 30 s. PP reflects the highest possible muscle power during cycling and MP,
local muscle endurance.
Physical Activity
An interviewer-administered 7-day activity recall questionnaire (31) was used to assign one of the following activity levels to the subject:fully sedentary, a little active,
nonnally active, very active, and competitive athlete. This questionnaire had been
found reliable, when administered twice, 1 week apart. It has a reasonable validity
when compared against heart rate monitoring (31) and direct observations (34).
Pubertal Development
Tanner Stage (pubic hair for boys and breast development for girls) was determined by having subjects look at a picture card and point to what stage of sexual
maturation (Tanner Stage 1-5) most appropriately described them. Such self assessment has recently been found highly valid when compared with experts' assessment (20).
Statistical Analysis
A 2 x 2 ANOVA was done to determine effects of birthweight and of gender on the
performance variables; The levekuf -significancewas taken a s p < .05.
Muscle Function and Low Birthweight - 331
Results
Anaerobic performance, muscle strength, lung functions, and activity scores are
summarized in Table 2. Birthweight affected significantly PP kg-' ( F = 16.48, p =
.0003) and MP kg-' ( F = 5.45, p = .03). There was also a near-significant difference
for PP ( F = 3.28, p = .08) and for MP ( F = 3.66, p = .06). Gender had a significant
effect on MP kg-' ( F = 5.45, p = .03) and on MP per LTV ( F = 5.12, p = .03). For
none of the variables was there a significant interaction between birthweight and
gender.
Among the females, the ELBW girls scored lower than their NBW controls
in PP (p = .046), PP kg-' (p = .04), PP per LTV (p = .03), FVC Cp = .048) and FEV,
(p = .02). Among the males, the ELBW boys scored lower in PP kg-' (p = .36) and
near significantly ( p = .059) in MP per LTV. Figure 1 summarizes individual scores
for PP kg-', combining the females and the males. A similar pattern was apparent
for MP kg-'.
In contrast to the anaerobic cycling performance, isokinetic muscle extension and flexion did not differ between birthweight or gender groups, nor was there
any interaction between group and gender. Similarly, there was no inter-group difference in the activity level. Within the female group, FVC and FEV, were lower
among the ELBW group ( p = .048 and .016, respectively).
Discussion
This study is the first to analyze anaerobic muscle performance of extremely low
birthweight individuals in their second decade of life. It suggests that some muscle
functions are still deficient at that stage, even when there are no overt clinical
manifestations of a neuromuscular deficiency. The present findings, therefore, extend previous reports about deficient motor performance in ELBW children at
their first decade of life. Of particular relevance is the study by Falk et al. (7) in
which 5- to 8-year-old ELBW children had a lower anaerobic performance, using
a modified Wingate test, than did those with normal birthweight or with very low
birthweight (1,000-1,499 g). A similar deficiency was found among 5- to 7-yearold ELBW children who performed the Wingate test (16).
The question of whether exercise performance of low birthweight children
is still deficient during the second decade of life may have practical importance.
For example, it may have implications for the young person's lifestyle and social
integration, as well as for the need for physical therapy and remedial training. Our
study suggests that some, but not all, ELBW individuals have a low performance
in anaerobic muscle performance. However, to address "residual deficiency" one
should conduct a longitudinal follow up of ELBW children over several years.
Powls et al. (26) tested at ages 6, 8, and 12-13 years a cohort of children born at
less than 1,250 g. While there was an improvement in gross motor function (using
a Test of Motor Impairment) between ages 6 and 8 years, there was no further
improvement at age 12-13. Thirty-four percent of the 12- to 13-year-old sample
had "clinically important" or "borderline" impairment, compared with 5% of normal birthweight controls. Our study did not include motor performance testing,
and we cannot tell whether ELBW subjects who had low anaerobic performance
also had motor impairment. It is noteworthy, though, that performance in the Wingate
test correlates with gross motor function in 7- to 14-year-old patients with cerebral
Table 2 Muscle and Pulmonary Functions and Activity in NBW and ELBW Subjects
Males
Variable
NBW
Females
ELBW
NBW
All
ELBW
NBW
ELBW
p p (W)
PPIKG (Wkg)
P P r n (WL)
MP (W)
MPKG (Wkg)
MPLTV (WL)
Extension strength (Nm)
Flexion strength (Nm)
Fvc (L)
FEV (Lls)
Activity level
+
Note. Values are expressed as M SD. NBW = normal birthweight. ELBW = extremely low birthweight. PP = peak power. MP = mean power.
Muscle Function and Low Birthweight - 333
PI
4
NBW
ELBW
Figure 1 -Anaerobic peak power (PP) per kilogram body mass in normal birthweight
(NBW) and extremely low birthweight (ELBW) adolescents. Individual data are presented for girls (circles) and boys (triangles) combined.
palsy (24). Specifically, a correlation of .80 (n = 23) was found with the walking,
running, and jumping components of the Gross Motor Function Test (27). More research is indicated to address the long-term muscle function-relatedsequelae of ELBW.
Only some of the differences in anaerobic performance were found significant. This may reflect the small sample size in this study. The statistical power of
the six anaerobic indices, as listed in Table 1, ranged from 0.55 (PP, W) to (0.98
(PP per kg). In order to achieve a power of 0.80 for PP, for example, we would
have needed 32 participants in each of the birthweight groups, instead of 17. Another limitation is the wide range of ages and maturational stages. One might assume that carry-over of functional deficiencies would diminish as the child goes
through puberty. However, even though the girls in this study were more mature
than the boys (Table I), the birthweight-related functionaldeficiencies were greater
among the girls. More studies are indicated in which the carry-over of such deficiencies can be assessed in more discrete age and maturational groups.
The contrast between a deficient anaerobic cycling performance and lack of
differences in isokinetic strength may be explained by differences in the complexity
of the two tasks. Cycling at maximal speed, as in the anaerobic test, requires coordination between and within various muscle groups of the thigh and the calf over three
joints. In contrast, a single knee extension or flexion requires mostly the contraction
of a single muscle group (with some contribution by postural trunk muscles) over one
joint. We suggest therefore that the low muscle power of the ELBW group results, at
least in part, from a deficient motor control. Indeed, previous studies have shown a
deficient gross and fine motor function in patients with ELBW or VLBW.
For example, Nickel et al. (21) examined school-age ELBW children, using
the Motor Test of Impairment and the Motor Accuracy Subtest of the Southern
California Sensory Integration Test. Nineteen of the 25 children had impaired gross
and fine motor skills. In a study of 5- to 7-year-old VLBW children, Largo et al.
(18) reported deficient fine motor ability (finger apposition), gross motor movements
334 - Small et a/.
(hopping on both legs), and other movements associated with diadochokinesis.
Pohlman and Isaacs (25) found several motor skill deficiencies in 5- to 9-year-old
children born at less than 2,200 g. Two recent studies (7, 15) have shown that the
maximal cycling speed against "zero" force in 5- to 8-year-old children of ELBW is
deficient compared with NBW controls. Motor skills can be deficient even if a low
birthweight child has no overt manifestations of a physical disability (5,7, 15), as is
the case with the subjects of the present study. Based on the above evidence, we
propose that low performance in the Wingate test, as found in this study, may reflect
a deficient neuromotor control and not only a low rate of anaerobic energy metabolism.
Deficiency in muscle function can result from quantitative factors such as a
small muscle size and cross-sectional area, as seen for example in an atrophic
muscle. Indeed, performance in the Wingate test among healthy adolescents (4)
and those with a neuromuscular disease (33) is correlated with their lean limb
mass. In the present study, lean thigh volume was similar in the two birthweight
groups. We, therefore, propose that the difference in anaerobic performance are
unlikely due to muscle size.
Low anaerobic muscle performance, like any other fitness component, could
result from physical hypoactivity (2). Insufficient activity can induce, for example,
disuse atrophy, which would affect anaerobic performance (2,23). Findings derived
from a 7-day interviewer-administered questionnaire in this study (Table 2) do not
suggest, though, that the ELBW were less active than their NBW counterparts.
It is unclear why the inter-group performance differences were more profound among the girls than the boys. The two ELBW gender groups did not differ
in the degree of prematurity (gestational age of 26.4 weeks in the girls and 27.1 in
the boys), nor in their birthweight (833 g in the girls vs. 824 g in the boys). Likewise, the females did not seem to have had a more severe perinatal outcome, as
judged from the number of days with respiratory support (36.5 days for the males
and 30.4 days for the females), number of days on supplementary oxygen (50 and
41.9 days, respectively), and rate of diagnosed BPD (50% in the males and 33% in
the females). One inter-gender difference is the lower body size (height and, insignificantly, body mass) of the ELBW females. As stated above, however, the lower
anaerobic performance of this group prevailed even when calculated per kilogram
body mass or lean thigh volume. We, therefore, cannot propose a valid explanation
for the relatively poorer performance of the ELBW girls based on our own data.
One possible explanation may be inferred from a study by Powls et al. (26):
Among 12- to 13-year-old low birthweight children, there were higher motor impairment scores in girls than in the boys. The authors could not explain the above
gender difference on the basis of perinatal clinical course. Another gender-related
difference in the present study was the low FVC and FEV, in the ELBW girls, but
not in the ELBW boys. However, this seeming deficiency in lung functions among
the ELBW girls virtually disappeared when FVC and FEV, were calculated as
percentage of norm for height (94% in NBW and 92% in ELBW for FVC and 97%
vs. 92%, respectively, for FEV,).
In conclusion, studies to date have shown a difference in anaerobic performance between NBW and ELBW 5- to 8-year-old children. This study is the first
to document deficiencies in some indices of anaerobic performance in the second
decade of life. These, most probably, result from subtle deficiencies in motor control. The fact that such sequelae can be detected as late as mid-puberty suggests
that they do not merely reflect a transitory delay in motor development. More
Muscle Function and Low Birthweight - 335
research is needed to study possible mechanisms for the low anaerobic muscle
performance associated with low birthweight.
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