Pediatric Physical Therapy:
A Longitudinal Evaluation of Maturational Effects on Lower Extremity Strength in Female Adolescent Athletes
Quatman-Yates, Catherine C. DPT, PhD; Myer, Gregory D. PhD, CSCS*D, FACSM; Ford, Kevin R. PhD, FACSM; Hewett, Timothy E. PhD, FACSM
Sports Medicine Biodynamics Center and Human Performance Laboratory (Drs Quatman-Yates, Myer, Ford, and Hewett), Cincinnati Children's Research Foundation, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio; Division of Occupational and Physical Therapy (Dr Quatman-Yates), Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio; Athletic Training Division, School of Allied Medical Professions (Dr Myer), The Ohio State University, Columbus, Ohio; Division of Molecular Cardiovascular Biology (Drs Ford and Hewett), Cincinnati Children's Research Foundation, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio; Departments of Pediatrics and Orthopaedic Surgery (Drs Myer and Hewett), College of Medicine, University of Cincinnati, Cincinnati, Ohio; Department of Rehabilitation Sciences (Dr Hewett), College of Allied Health Sciences, University of Cincinnati, Cincinnati, Ohio; Departments of Physiology and Cell Biology (Dr Hewett), School of Biomedical Science, College of Medicine, The Ohio State University, Columbus, Ohio; Sports Medicine Center (Dr Hewett), Orthopaedic Surgery and Biomedical Engineering and Sports Health Institute, Cincinnati Children's Research Foundation, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio.
Correspondence: Catherine C. Quatman-Yates, DPT, PhD, Sports Medicine Biodynamics Center and Human Performance Laboratory, 3333 Burnet Ave, MCL 10001, Cincinnati, OH 45229 (Catherine.firstname.lastname@example.org).
Grant support: The study was supported by funding from the National Institutes of Health grants R01 AR04973505-01, R01 AR055563-02, and R03-AR057551.
There are no potential conflicts of interest regarding this article.
Purpose: Recent studies demonstrate that adolescent growth without corresponding strength adaptations may lead to the development of risk factors for patellofemoral pain and anterior cruciate ligament injuries. Our purpose was to investigate the longitudinal trajectories of lower extremity strength across maturational stages for a cohort of female student athletes.
Methods: A nested cohort design was used to identify 39 subjects who had complete knee flexion, knee extension, and hip abduction strength data for 3 test sessions spaced approximately 1 year apart and during which they transitioned from prepubertal to a pubertal status.
Results: Knee extension strength increased while hip abduction and hamstrings-to-quadriceps ratio strength decreased from prepubertal to pubertal stages (P < .05). No effects of time with respect to knee flexion strength or nondominant/dominant limb differences were found (P > .05).
Conclusion: These data provide support that preadolescence is an optimal time to institute strength training programs aimed toward injury prevention.
INTRODUCTION AND PURPOSE
Recent evidence indicates that 2 common lower extremity musculoskeletal conditions increase in incidence among young athletes during adolescence: injuries to the anterior cruciate ligament (ACL) and patellofemoral pain (PFP) syndrome.1–3 Although ACL injuries and the emergence of PFP increase for both males and females around the time of puberty and throughout adolescence, females sustain ACL injuries at least 4 to 6 times more frequently4–6 and are affected by PFP 2 to 10 times more often than their male counterparts.7,8 Both ACL injuries and PFP are associated with pain and significant reductions in activity levels during acute recovery phases.9 Both conditions have also been linked to amplified risk for reinjury/recurrence and degenerative joint pathology.3,10–13 Moreover, the lifelong effect these conditions may have on a person's future risk profile is underscored by the potential to trigger a downward spiral of health concerns that begins with pain and decreased activity levels and over time can lead to poor cardiovascular fitness, obesity, and diabetes.14,15 Therefore, a thorough understanding of the underlying pathomechanics that lead to increased incidence of PFP and ACL injuries during adolescence could considerably enhance clinicians’ ability to identify and address the risk factors that predispose young athletes to these conditions and the associated long-term sequelae.
A number of studies demonstrate that musculoskeletal growth during puberty in the absence of corresponding neuromuscular adaptation in athletes may facilitate the development of known risk factors for ACL injuries and PFP such as hamstrings-to-quadriceps strength imbalances, hip weakness, and decreased neuromuscular control of the knee.1,3,16–19 Differences between males’ and females’ neuromuscular performance in many of these same variables have been reported to begin to emerge around the time of pubertal maturation.17,18,20,21 These sex-specific developmental changes and resultant divergence in neuromuscular profiles may be associated with the disparity in incidence of ACL injury and PFP between the sexes during adolescence and perhaps indicative of an optimal window of opportunity for prevention and treatment of these injuries and disorders.
The purpose of this study was to investigate the longitudinal trajectories of lower extremity strength (defined here as muscle power at a constant velocity normalized to body mass) across maturational stages for a cohort of female adolescent student athletes. It was hypothesized that as subjects progressed from prepubertal to pubertal and late/postpubertal levels, deficits in hip abduction and hamstring-to-quadriceps strength would emerge. The results of the study are discussed relative to known risk factors and potential prevention strategies for ACL injuries and PFP in female adolescents.
A nested longitudinal cohort design was used to identify subjects from a prospectively collected, longitudinal pool of anthropometric, biomechanical, and maturational data for a large geographical cohort of female adolescent soccer and basketball players (n = 709). Entire teams were brought in at the beginning and end of each season for testing sessions, and longitudinal data were collected for all subjects. However, successive year-to-year data were available only for subjects who did not graduate and made the team roster in consecutive years. To be included in this study, subjects had to meet the following inclusion criteria: (1) have complete data for 3 test sessions spaced approximately 1 year from the previous visit; (2) be classified as “prepubertal” for at least 1 visit on a modified Pubertal Maturation Observational Scale (PMOS); (3) have at least 1 visit in which the PMOS rating had transitioned to “pubertal”; and (4) have no history of knee, hip, back, or ankle surgery.
The study was approved by the Institutional Review Board, and informed written consent was obtained from both the child and a parent or guardian prior to data collection. A total of 39 subjects were identified as having 3 consecutive testing sessions that occurred approximately 12 months (12.0 ± 0.1 months) apart that corresponded with the start of the athlete's athletic season each year and met all additional inclusion criteria. All subjects who met the study's criteria were soccer players as there was no prepubertal data for any of the basketball players. Table 1 provides a summary of the demographic information for subjects at each pubertal stage.
At each testing session, subjects’ body mass and height were measured using a calibrated physician scale and a stadiometer while subjects stood with bare feet. Subjects were asked to identify which leg they would prefer to use to kick a ball as far as possible. The leg each subject identified as the preferred kicking leg was recorded as the dominant lower limb. Also, during each testing session, the modified PMOS was used to classify subjects into 1 of 3 maturational categories: prepubertal (approximately Tanner stage 1), early pubertal (approximately Tanner stages 2 and 3), and late/postpubertal (approximately Tanner stages 4 and 5). The modified PMOS includes both parental questionnaires and an observational questionnaire completed by an investigator.22,23 The questionnaires are composed of questions related to the development of secondary sex characteristics associated with puberty such as acne, recent growth spurt, sweating after physical activities, evidence of muscular development, darkened underarm hair, onset of menarche, and breast development. The original PMOS was modified on the basis of recommendations from specialists in adolescent health to include a more specific breakdown the item of “has begun menarche” to a more precise weighting of “the adolescent began menarche less than 1 year ago, 1 to 2 years ago, or greater than 1 year ago” as well as to include additional questions regarding height of biological parents to calculate percentage of adult stature. The PMOS has demonstrated good reliability and has been used successfully in previous studies to differentiate between different pubertal stages.16,23,24
An isokinetic dynamometer was used to measure peak isokinetic torque production of the knee flexors, knee extensors, and hip abductors. For the knee flexors and knee extensor tests, subjects were seated on the dynamometer with the trunk perpendicular to the floor, the hip flexed to 90°, and the knee flexed to 90°. A 5-repetition knee extension-flexion warm-up at 300° per second for each leg was performed prior to the test. The recorded test session consisted of 10 repetitions of knee extension-flexion with each limb at 300° per second. This speed and the number of repetitions were selected on the basis of previous studies using a similar protocol that investigated knee injury risk factors.25–28 For the hip abduction test, subjects were placed in a standing position facing the dynamometer head and secured with a strap around the waist just above the iliac crest. The dynamometer head was positioned so that the axis of rotation of the dynamometer aligned with the center of rotation of the hip. Subjects performed 5 maximum effort repetitions at a speed of 120° per second. This speed was determined on the basis of pilot testing that determined that 120° per second could be comfortably executed in the standing position and still approximate actual hip abduction/adduction velocities that occur during high-risk cutting tasks. Intrarater reliability using a single investigator for these methods has been demonstrated to be good to excellent with intraclass correlation coefficients of 0.86 on the left (CI: 0.58-0.97) and 0.92 on the right (CI: 0.727-0.984).29 These methods have been used previously to investigate hip strength in female adolescent athletes.30,31 Peak torques for all test repetitions were recorded for knee flexion, knee extension, and hip abduction. Subsequently, all peak torque values were normalized to each subject's body mass (Nm/kg).
To align subjects according to maturational status rather than by chronological age or visit number, a spreadsheet was created for each variable and arranged according to pubertal status. The first testing session where a subject was classified with a pubertal status essentially became time point 0 (labeled as “pubertal”). All variables were graphed longitudinally for 1 year before puberty through 1 year after first being classified as pubertal (labeled as “late/postpubertal”). Statistical analysis was also performed for the prepubertal, pubertal, and late/postpubertal categories.
Two-way repeated-measures analysis of variances with 3 time levels and 2 levels for leg (dominant limb compared with nondominant limb) were conducted for knee extensor (quadriceps) strength, knee flexor (hamstrings) strength, hamstrings-to-quadriceps strength ratio, and hip abductor strength. The alpha level was set a priori at α < .05 with a Bonferroni adjustment made for multiple comparisons.
Figure 1 provides a graph of the strength trajectories (mean of the dominant and nondominant limbs) for each strength variable across pubertal stages. Statistically significant effects for time were observed for knee extensor strength, hamstrings-to-quadriceps strength ratio, and hip abductor strength (P < .05). No effects for time were found for knee flexion strength or for dominant to nondominant limb differences for any of the strength measures (P > .05). Table 2 provides subjects’ 95% confidence intervals for the means of each strength variable at each of the pubertal stages.
Pairwise comparison tests indicated a statistically significant increase (mean change; 95% confidence interval) in knee extensor strength from prepubertal to pubertal status (0.073; 0.00–0.146 Nm/kg) and from prepubertal to late/postpubertal (0.119; 0.066–0.172 Nm/kg), but no statistically significant change from pubertal to late/postpubertal (0.046; −0.118 to 0.026 Nm/kg). Pairwise comparison tests for hamstrings-to-quadriceps ratio demonstrated a statistically significant decrease for prepubertal to pubertal (0.071; 0.000–0.143 Nm/kg) and from prepubertal to late/postpubertal (0.109; 0.034–0.184 Nm/kg) but no statistically significant change from pubertal to late/postpubertal (0.038; −0.028 to 0.103 Nm/kg). Likewise, pairwise comparison tests indicated a statistically significant drop in hip strength from prepubertal to pubertal (0.171; 0.069–0.272 Nm/kg) and from prepubertal to late/postpubertal (0.290; 0.119–0.461 Nm/kg) but no significant change in hip strength was observed from pubertal to postpubertal (0.119; −0.21 to 0.260 Nm/kg).
The purpose of this study was to investigate the longitudinal trajectories of lower extremity strength normalized to body mass across maturational stages for a cohort of female adolescent student athletes. It was hypothesized that as subjects progressed from prepubertal to pubertal and late/postpubertal levels, deficits in strength relative to body mass would emerge. The results from this study provide evidence that while knee extension strength relative to body mass steadily increases throughout maturation, knee flexor strength remains about the same. This leads to an increased imbalance in hamstring-to-quadriceps strength. The results from this study also indicate that female adolescents may experience a significant regression in hip abduction strength relative to body mass in the year they transition from prepubertal to pubertal status. Collectively, these results indicate that imbalances in lower extremity activation and strength relative to body mass emerge during puberty for female athletes.
Patellofemoral pain is a painful condition that peaks in incidence during the middle school years3 and eventually affects nearly 1 of 4 school-aged youth.32 Likewise, ACL injuries in females have higher rates following the onset of the pubertal growth spurt.2 Although ACL injuries and the emergence of PFP increase for both males and females around the time of puberty, females sustain ACL injuries and experience PFP at least 4 to 6 times more frequently4–6 and are affected by PFP 2 to 10 times more often than their male counterparts.7,8 Altered or reduced control of the limbs during physical activities may result in excessive knee abduction joint loads in females. This neuromuscular dysfunction appears to increase risk of acute ACL injury and chronic PFP in females.3,25,33,34 Deficits and imbalances in lower extremity strength have also been linked to both ACL injury and PFP.3,25,28,32 The timing of the emergence of these deficits appears to coincide with the emergence of strength imbalances for female adolescents during puberty. Thus, the results of this study may provide a potential explanation for the timing of increased incidences of PFP and ACL injury observed in female adolescents.
The rapid increases in height and body weight adolescents experience during puberty have led to many hypotheses that link pubertal maturation to concomitant decreases in motor control and subsequently increased risk for sports and recreation-related injuries. However, past studies related to these hypotheses have yielded inconsistent results. For example, Davies and Rose23 found no evidence for impaired coordination during puberty, while Loko et al35 found that female adolescents exhibited plateaus and regressions in a number of motor abilities. Findings from a recent systematic review indicate that many of the inconsistencies in our understanding of the relationship between maturation and motor control abilities may relate to a number of methodological limitations and incongruities.36 For example, a number of previous studies have used motor skill performances (eg, throwing distance and accuracy, vertical jump, and running speed) as measures of motor control.23,35,37 However, the use of motor skill performances as indicators of motor control abilities can be problematic because skill performance levels can be strongly influenced by confounding variables such as experience and type of measurement. Other common limitations in studies on maturation and motor control include operational definitions of maturation groups based on chronological age groupings, the combination of males and females within a single-subject pool, and a lack of longitudinal follow-ups on subjects across the pubertal process. These types of operational definitions and subject-pooling strategies can mask progression and regression trends because of the wide variability in maturational status of adolescent children of the same chronological age and potential sex-specific disparities.18,19,38–41
To address limitations in previous studies, this study incorporated several important design features: (1) motor control variables related to neuromuscular strength rather than motor skill variables were used, (2) multiple potential confounding sex-specific disparities were accounted for through the inclusion of only females, (3) pubertal stages were used instead of chronological age groups to minimize error due to the wide variability in age at onset of puberty, and (4) longitudinal follow-ups that covered a single group of subjects across multiple pubertal stages were used for analyses instead of cross-sectional data. The longitudinal nature of the design and use of pubertal stages were particularly useful for identifying specific points in the maturation process where strength deficits might be expected to emerge. For example, hip abductor strength appears to undergo a fairly rapid change relative to body mass during the year when females transition from prepubertal to pubertal status. Imbalances between hamstring and quadriceps strength, on the contrary, appear to emerge more gradually over the 3-year period leading from prepubertal to late/postpubertal status.
The results from this study and other studies indicate that a potential window of opportunity may exist for the optimal initiation of integrative neuromuscular training based on measures of somatic maturity. Specifically, the most beneficial and thus desirable time to initiate integrative training programs may be during preadolescence prior to the period of obvious pubertal maturation when youth are growing most rapidly. Children with earlier somatic maturation (growth) may particularly benefit from earlier participation in integrative neuromuscular strength training.14,42 In a recent longitudinal study, Ford and colleagues19 noted that pubertal females had an increased change in abnormal landing mechanics over time. In addition, important contributing risk factors for knee injury were significantly greater across consecutive years in young postpubertal female athletes compared with males. Integrative neuromuscular training programs have been successful at reducing these abnormal biomechanics43–46 and appear to decrease PFP and ACL injury rates in female athletes.47,48
One limitation of this study is that all of the subjects in this study were females. There is evidence to suggest that males and females may differ in the strength and neuromuscular control abilities that are present during puberty.18–20,49,50 In addition, the longitudinal nature of this study may have been limited by the nature of the design in that the subjects with data that were available for 3 consecutive years were all athletes that made the school team for multiple years. Therefore, future studies should include males and nonathletes to determine the generalizability of these results beyond female adolescent athletes.
The findings of this study indicate that hamstring and quadriceps strength deficits and imbalances between hamstrings and quadriceps strength appear to emerge during pubertal maturation. As these strength variables have been linked to increased risk for ACL injury and PFP, these data provide further support that preadolescence may be an optimal time to institute programs aiming to reduce deficits (eg, increased knee abduction motion and load) that accelerate during maturation and lead to increased musculoskeletal injury risk in female adolescents.
The authors thank Dr Mark Paterno, Dr Carmen Quatman, Dr Laura Schmitt, Chad Cherny, Jensen Brent, Kim Foss, and Staci Thomas for their assistance with data collection and other aspects of the study.
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adolescent; female; puberty/physiology; strength
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