Abstract
Background: Compared with male athletes, female athletes demonstrate
increased dynamic valgus angulation of the knee during landing from a jump,
although prior to maturation male and female athletes have similar forces and
motions about the knee when they land from a jump. Our hypothesis was that
musculoskeletal changes that accompany maturation result in poor neuromuscular
control of the knee joint in female athletes.
Methods: One hundred and eighty-one middle-school and high-school
soccer and basketball players—100 girls and eighty-one
boys—participated in the study. Dynamic control of the knee joint was
measured kinematically by assessing medial knee motion and the lower-extremity
valgus angle and was measured kinetically by assessing knee joint torques; the
values were then compared between female and male athletes according to
maturational stage. Lower-extremity bone length was measured with
three-dimensional kinematic analysis.
Results: Following the onset of maturation, the female athletes
landed with greater total medial motion of the knees and a greater maximum
lower-extremity valgus angle than did the male athletes. The girls also
demonstrated decreased flexor torques compared with the boys as well as a
significant difference between the maximum valgus angles of their dominant and
nondominant lower extremities after maturation.
Conclusions: After girls mature, they land from a jump differently
than do boys, as measured kinematically and kinetically.
Clinical Relevance: Following the onset of the pubertal growth
spurt, female athletes change the way that they land from a jump. This change
may be due to decreased neuromuscular control of the knee and may explain why
the risk of anterior cruciate ligament injury is higher in girls than it is in
boys. The measures of neuromuscular control of the knee used in this report
may be employed to monitor athletes and to direct appropriate new
interventions to athletes at high risk for injury.
Although girls and boys have an equal number of ligament sprains prior to
adolescence, girls have a higher rate immediately following their growth spurt
and into maturity1.
Michaud et al. reported that the Tanner stage of maturation of girls was
associated with the occurrence of sports
injuries2.
Adolescent girls who participate in pivoting and jumping sports have a four to
sixfold greater rate of injuries of the anterior cruciate ligament than do
adolescent boys participating in the same
sports3-5.
In contrast, an analysis of the published
literature6-9
demonstrated no evidence of a difference in the rates of anterior cruciate
ligament injury between prepubertal male and female athletes.
Neuromuscular patterns in males and females diverge substantially during
maturation. Males demonstrate increases in power, strength, and coordination
with age that correlate with their maturational stage, whereas, on the
average, girls show little change throughout
maturation10,11.
For example, the vertical jump height demonstrated by boys increases steadily
during maturation, but that demonstrated by girls does
not10,11.
One of us (T.E.H.) and
colleagues4 tracked
the occurrence of anterior cruciate ligament injuries in 1263 athletes through
their soccer, volleyball, and basketball seasons. Untrained girls had
significantly higher rates of anterior cruciate ligament injury than did
trained girls and boys (p < 0.05), whereas the rates in trained girls were
not different from those in untrained boys. That prospective study
demonstrated that neuromuscular training has the potential to decrease rates
of anterior cruciate ligament injury in adolescent female athletes. Intensive
neuromuscular training may induce a so-called neuromuscular spurt that would
otherwise be absent in adolescent
girls12-14.
Neuromuscular control of the knee can be defined as the unconscious
response to an afferent signal concerning dynamic knee joint
stability15. The
absence of neuromuscular control of the knee joint may be responsible for the
increased rates of knee injury in
females14,16,
but it is not normally measured in athletes prior to participation in sports.
Standard preparticipation physical examinations assess static measures of
joint stability. Few if any dynamic measures are assessed, and intervention is
rarely implemented. Although musculoskeletal disorders are observed during
approximately 10% of preparticipation examinations of athletes, intervention
is carried out for 1% to
3%15-18.
No method for the accurate and practical screening and identification of
athletes at increased risk for anterior cruciate ligament injury is currently
available.
Our long-term objectives are to determine how female athletes become more
susceptible to anterior cruciate ligament injury and to prospectively identify
those who are more susceptible in order to optimize the effectiveness of
interventions designed to prevent anterior cruciate ligament injuries. The
objectives of this study were to determine what role growth and development
play in the mechanism of decreased neuromuscular control of the knee and to
test methods to identify female athletes with decreased dynamic control of the
knee. We tested the hypothesis that musculoskeletal changes that accompany
maturation are associated with poor neuromuscular control of the knee in
female athletes.
Subjects
We performed a cross-sectional controlled laboratory study of eighty-one
healthy male and 100 healthy female preadolescent and adolescent athletes
(Table I). The subjects were
male and female basketball and soccer players from area middle schools and
high schools who had volunteered to participate in the study. Acceptance into
the study was based on predetermined inclusion and exclusion criteria: the
subjects had to be on a school-sponsored basketball or soccer team, and
athletes who had had a previous anterior cruciate ligament injury were
excluded. In each case informed written consent was obtained from both the
child and a parent, and the study was approved by the institutional review
board of the Cincinnati Children's Hospital Medical Center. After the informed
consent was obtained, the height, weight, and dominant lower limb were
recorded. The dominant lower limb was determined for each subject by asking
which limb he or she would use to kick a ball as far as possible. The tibial
and thigh lengths of each subject were measured with the three-dimensional
kinematic system described below and were recorded during the same laboratory
evaluation.
Table I provides data on the
six subject groups based on gender and stage of pubertal
development19. A
modified Pubertal Maturation Observational Scale (PMOS) was used to classify
subjects into maturational categories: prepubertal (equivalent to
Tanner20,21
Stage 1), early pubertal (equivalent to Tanner Stages 2 and 3), or late or
postpubertal (equivalent to Tanner Stages 4 and 5). The categories were then
analyzed both as groupings and as a continuous variable. The scale is based on
several indicators of pubertal maturation (growth spurt, menarchal status,
body hair, sweating, and muscular
definition)19. It
can be used to reliably classify subjects into developmental stages on the
basis of a parental report and the observations of an
investigator22. The
reliability of the scale has been demonstrated to be
high19.
Three-Dimensional Kinematic Analysis
A three-dimensional kinematic test was utilized as a measure of
neuromuscular control of the
knee23. Each
subject had twenty-three retroreflective markers placed on the sacrum and
bilaterally on the shoulder, anterior superior iliac spine, greater
trochanter, midpart of the thigh, medial and lateral aspects of the knee,
midpart of the shank, medial and lateral aspects of the ankle, and heel and
toe (between the second and third metatarsals). The motion analysis system
consisted of eight digital cameras (Eagle Cameras; Motion Analysis, Santa
Rosa, California) connected through an Ethernet hub to the data collection
computer (Dell Computer, Round Rock, Texas) and sampled at 240 Hz. Two force
platforms (AMTI, Watertown, Massachusetts) were sampled at 1200 Hz and time
synchronized to the motion analysis system. Data were collected with EVaRT
(version 3.21; Motion Analysis) and were imported into KinTrak (version 6.2;
Motion Analysis) for data reduction and analysis. Prior to each data
collection session, the motion analysis system was calibrated to manufacturer
recommendations.
A static trial was performed to align the joint coordinate system to the
laboratory. Subjects were instructed to stand still and were aligned as
closely with the laboratory coordinate system as possible. The medial knee and
ankle markers were subsequently removed prior to the drop vertical jump
trials. The drop vertical jump started with the subject standing on top of a
31-cm-high box with the feet positioned 35 cm apart, as measured between the
toe markers. The subject was instructed to drop directly down off the box and
immediately perform a maximum vertical jump, raising both arms as if he or she
were jumping for a basketball rebound (see
Appendix)24. The
two force platforms were embedded into the floor and positioned 8 cm apart so
that each foot came into contact with a different platform during the
maneuver. The first contact on the platforms (i.e., the drop from the box) was
used for analysis. Three successful trials were recorded for each subject.
The three-dimensional Cartesian marker trajectories from each trial were
estimated with use of the direct linear transformation method and were
filtered through a low-pass Butterworth digital filter at a cutoff frequency
(9 Hz) determined with residual
analysis25.
Varus-valgus knee-joint angles of the right and left limbs were calculated
from an embedded joint coordinate
system26. A
positive lower-extremity varus-valgus angle represented valgus, and a negative
angle represented varus. Vertical ground reaction force was used to identify
the time of the initial contact with the ground and of toe-off during take-off
from the jump. The lower-extremity knee angle at initial contact and the
maximum lower-extremity angle during stance (from initial contact to toe-off)
were recorded.
Medial knee motion was calculated bilaterally on the basis of the coronal
plane distance between the right and left lateral knee markers during the drop
vertical jump. The knee distance was recorded 0.03 second prior to the initial
contact and then as the minimum knee distance during the stance phase (maximum
medial motion)23.
The difference between the knee distance prior to the initial contact and the
minimum medial knee distance was calculated as the total medial knee motion
(in centimeters) and as the medial knee motion normalized to body height (in
centimeters). All kinematic data were ensemble averaged from three trials.
Isokinetic Dynamometer Strength Measures
An isokinetic dynamometer was utilized to measure peak isokinetic torque
production of the hamstrings and quadriceps muscles in order to assess knee
flexion and extension strength. Subjects were seated on the dynamometer with
the trunk perpendicular to the floor, the hip flexed to 90°, and the knee
flexed to 90°. They performed a five-repetition knee extension-flexion
warm-up with each lower limb at 300°/sec prior to the test. The test
session consisted of ten repetitions of knee extension-flexion with each limb
at 300°/sec. Maximum knee flexion and extension torques were recorded.
Reliability Measurements
Studies of the reliability of the measurements of the limb-segment lengths,
the three-dimensional kinematic testing, and the dynamometric measurements
were conducted. All measures demonstrated high day-to-day reproducibility in
the laboratory. The three test sessions were one or two days apart and were
held at approximately the same time of day. The testing order was randomized
for each subject. The three-dimensional system has a marker tracking error of
approximately 0.2 mm. The reliability of all measurements was high. The
intraclass correlation coefficients were high for the lengths of the dominant
and nondominant shanks and thighs measured over three different days (five
subjects, intraclass correlation coefficient = 0.964 for the shank
measurements and 0.954 for the thigh measurements). The between-day
reliability of the three-dimensional motion analysis and isokinetic
dynamometer measurements was assessed in the same sample of subjects. The
intraclass correlation coefficient was 0.916 for the reliability of the
measurement of the knee distance at the time of maximum medial motion, 0.893
for total medial motion, and 0.848 and 0.968 for isokinetic dynamometer
measures of peak hamstrings and quadriceps torque.
Statistical Analysis
The means and standard error of the mean for each variable were calculated
for each subject group. An analysis of variance test was used to compare means
between the different groups, and a Fisher least-significant-difference post
hoc test was used to determine significant differences between groups (p <
0.05). A paired t test was used to determine significant differences between
the dominant and nondominant sides (p < 0.05). For measures of relative
correlation between parameters, the Pearson correlation coefficient was
calculated. Statistical analyses were conducted with SPSS for Windows software
(release 10.0.7; SPSS, Chicago, Illinois).
Increases in Lower-Limb-Segment Lengths in Female and Male
Athletes
The shank and thigh lengths of the girls and boys in the early pubertal and
late or postpubertal stages were increased relative to those of their
prepubertal counterparts (p < 0.01; see Appendix). In addition, the shank
and thigh lengths of the girls and boys in the late or postpubertal stage were
increased relative to those of the girls and boys in the early pubertal stage
(p < 0.01). Height and weight increased in these populations in a similar
fashion, although the increases were smaller in girls than in boys. In order
to correct for the potentially confounding effects of height and weight
differences between groups, neuromuscular measures were normalized to height
and weight.
Increases in Medial Knee Motion in Female Athletes with Growth and
Development
Three-dimensional motion analysis demonstrated no differences in medial
knee motion between boys and girls prior to the onset of maturation
(Fig. 1). The maximal medial
knee motion demonstrated by the girls in the prepubertal and early pubertal
stages was similar to that demonstrated by the boys in those stages. However,
the girls in the late or postpubertal stage displayed significantly more
medial knee motion than did the boys in that stage (p < 0.01) and the girls
and boys in the prepubertal and early pubertal stages (p < 0.05). Medial
motion of the knees correlated with shank (tibial) length in the female
athletes (r = 0.37, p < 0.001) but not in the male athletes (r = 0.07, p =
0.53).
The lower-extremity valgus angle at initial contact and the maximum angle
during landing are displayed in Figure
2. The girls in the late or postpubertal stage displayed a greater
lower-extremity valgus angle than did the boys in that stage, both at initial
contact (5° ± 1° compared with 1° ± 1°; p <
0.01) and at maximum during landing (30° ± 3° compared with
19° ± 3°; p < 0.01). Girls in the late or postpubertal stage
also displayed a greater lower-extremity valgus angle at initial contact than
did both the prepubertal girls (2° ± 2°; p < 0.05) and the
girls in early puberty (1° ± 1°; p < 0.01), and they
displayed a greater maximum angle than did the prepubertal girls (14°
± 4°; p < 0.01) and the girls in early puberty (20° ±
3°, p < 0.05).
Side-to-Side Differences in Valgus Angle in Female Athletes at
Landing
The maximum lower-extremity valgus angle during landing was significantly
lower on the nondominant side than it was on the dominant side in the girls in
the late or postpubertal stage (p < 0.01,
Fig. 3).
Increases in Knee Muscle Peak Torque with Maturation in Male but Not
Female Athletes
After normalization to body weight, isokinetic dynamometer measurements
demonstrated that male athletes had significantly greater hamstrings peak
torques with increasing maturity, whereas peak torque remained steady with
increasing maturational stage in female athletes. Boys demonstrated
significantly higher hamstrings peak torque in the late or postpubertal stage
than they did in the early and prepubertal stages (p < 0.05), whereas, with
the numbers available, girls demonstrated no differences in hamstrings peak
torque across maturational stages (Fig.
4). Hamstrings peak torque correlated with femoral length in both
male (r = 0.69, p < 0.001) and female athletes (r = 0.57, p < 0.001).
However, hamstrings peak torque was significantly lower in the girls in the
prepubertal (p < 0.01), early pubertal (p < 0.05), and later or
postpubertal (p < 0.01) stages than it was in the boys in the same
stages.
Male athletes also demonstrated significantly greater quadriceps peak
torque (normalized to body weight) with increasing maturity, whereas girls did
not (Fig. 5). The male athletes
demonstrated significantly higher quadriceps peak torque in the late or
postpubertal stage than they did in the early and prepubertal stages, whereas,
with the numbers available, the girls demonstrated no differences in
quadriceps peak torque across maturational stages. Quadriceps peak torque
correlated with femoral length in both male (r = 0.78, p < 0.001) and
female athletes (r = 0.57, p < 0.001). However, compared with boys in the
same maturational stage, girls had a 12% deficit in quadriceps peak torque
(normalized to body weight) in the prepubertal stage (p < 0.05), an 11%
deficit in the early pubertal stage (p < 0.05), and an 18% deficit in the
late or postpubertal stage (p < 0.001).
Changes in Neuromuscular Control of the Knee in Adolescent
Athletes
Several authors have documented a substantial increase in neuromuscular
strength and coordination following the growth spurt in adolescent boys but
not in the average adolescent
girl27-30.
Gender differences have been documented for grip strength, pulling strength,
vertical jumps, long jumps, sprint speed, and balance in both longitudinal and
cross-sectional studies. In a recent cross-sectional study by Kellis et
al.10, female
basketball players did not increase vertical jump performance with increasing
age, whereas male players improved their scores with age.
The data in the literature demonstrate that the genders diverge with regard
to neuromuscular performance and injury rate following peak height velocity,
which occurs at the age of eleven to twelve years in
girls20,21.
Differences in knee injury rates have been reported to occur at the age of
twelve. The observed changes in neuromuscular measures across maturational
boundaries were very different between the boys and girls in the present
study. Girls demonstrated decreased neuromuscular control of the knee from
early to late puberty, whereas boys demonstrated better neuromuscular control
of the knee in late puberty than they had in early puberty.
Changes in Landing from a Jump by Adolescent Athletes
This study supports the hypothesis that musculoskeletal changes that
accompany maturation are associated with poor neuromuscular control of the
knee in female athletes. We documented changes, following the onset of
maturation, in how girls and boys land from a jump. Boys regain neuromuscular
control following their so-called neuromuscular spurt, whereas girls do not
appear to make a similar neuromuscular adaptation. This potentially leads to
decreased dynamic knee stability in female athletes. In the prepubertal and
early pubertal stages, girls and boys displayed similar amounts of
lower-extremity valgus motion, but girls demonstrated more valgus motion than
boys at maturity. This study indicates that biomechanical changes during
maturation are likely to underlie the changes in neuromuscular control of the
knee.
Neuromuscular control indices in female athletes decreased with the onset
of puberty, and the decreases continued into the late or postpubertal stage.
This decrease may occur just prior to or coincident with the increase in
injury risk. Although one cannot predict the exact stage of development at
which the risk of injury will increase, it most likely does so subsequent to
the period of peak height velocity and decreased neuromuscular control of the
knee. Neuromuscular adaptation and coordination may lose pace with skeletal
growth at this
time31,32.
The timing of this transition should be the subject of careful, longitudinal
study.
Mechanisms of Anterior Cruciate Ligament Injury in Adolescent Female
Athletes
The findings of the current study suggest that boys use a more efficient
strategy for muscular damping of forces, through greater muscular
cocontraction. The observed increases in valgus motion of the knees of
postpubertal girls suggest altered muscular control of the lower extremities
in the coronal plane. This probably reflects changes in contraction patterns
of the adductors and abductors of the hip and the flexors and extensors of the
knee33,34.
Muscular contraction can decrease the valgus laxity of the knee
threefold35. The
present findings support the hypothesis that growth and development decrease a
female's neuromuscular control of the knee.
It has been estimated that >70% of all anterior cruciate ligament
injuries occur at landing from a
jump36. Jump
take-off and landing movements were evaluated biomechanically in the current
study. One of us (T.E.H.) and colleagues previously demonstrated that valgus
torques about the knee are significant contributors to landing forces from a
jump (p <
0.01)14.
Biomechanical differences in the net knee-joint torques, landing forces, and
muscle strength were found between male and female athletes during the
sports-specific, non-contact activities of jumping and
landing14. Landing
with the knee in valgus can potentially injure the knee, and athletes should
avoid excessive valgus or varus forces at the knee to minimize the risk of
knee injury34.
An athlete may be at risk for injury if the lower extremity is not properly
aligned or if the foot is in an unusual position when he or she lands from a
jump37. A multiple
regression analysis incorporating flexion angles, flexion and extension
moments, and valgus torque at the knee, hip, and ankle demonstrated that
valgus torques at the knee were the sole significant predictors of peak
landing forces (p <
0.01)14. It is
likely that more equal distribution of forces transmitted across both the
medial and the lateral compartment of the knee joint would lead to decreased
landing
forces14,38.
In addition, a decreased valgus or varus moment would decrease the risk of
femoral condylar lift-off from the tibial plateau. Biomechanical studies have
established the relationship between femoral condylar lift-off and injury
risk33,35.
Limitations of This Study
Several limitations of this study should be considered. Several possible
contributing and confounding variables, including school, team, age/grade,
aggressiveness, foot pronation, quadriceps angle, femoral notch width, and
blood hormone levels, were not controlled for in the study design. In
addition, the study was cross-sectional and, as such, could not assay for
changes over time; it was only a snapshot of one time-point. The hypotheses of
this study must be tested in future, prospective longitudinal studies to
better answer the questions raised by this investigation.
The fact that we included only soccer and basketball players in our study
limits the generalizability of its findings. However, gender differences in
injury incidence have been demonstrated in several sports, including
basketball, soccer, lacrosse, team handball, and volleyball. There are
probably differences in neuromuscular control measures in most gender-paired
sports. Therefore, the associations between pubertal stage and neuromuscular
control measures and injury in adolescent basketball and soccer players should
be comparable with those found in adolescent athletes participating in other
sports.
Future Directions
In conclusion, the findings of this study support our hypothesis that
musculoskeletal changes that accompany maturation are associated with poor
neuromuscular control of the knee in female athletes. These changes in height,
weight, and bone length, in the absence of neuromuscular adaptation to these
changes, may lead to dynamic knee instability in female athletes.
Our findings may lead to advances in the prevention and treatment of
anterior cruciate ligament injuries in young female athletes. We demonstrated
that growth and development play a role in the mechanism of decreased
neuromuscular control of the knee. Future research should focus on controlled
prospective longitudinal studies of defined populations of female athletes
followed through multiple sports seasons to correlate neuromuscular profiles
to injury risk. Only then can the relative injury risk be predicted with high
sensitivity.
Figures showing tibial and femoral length measurements in the athletes and
a video of adolescent male and female athletes landing from a jump are
available with the electronic versions of this article, on our web site at
(go to the article citation and click on "Supplementary Material")
and on our quarterly CD-ROM (call our subscription department, at
781-449-9780, to order the CD-ROM).
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