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Biomechanical and neuromuscular aspects of non-contact ACL injuries: The influence of gender, experience and training

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Biomechanical and neuromuscular aspects of non-contact ACL injuries: The influence of gender, experience and training

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Content BIOMECHANICAL AND NEUROMUSCULAR ASPECTS OF NON- CONTACT ACL INJURIES: THE INFLUENCE OF GENDER, EXPERIENCE AND TRAINING Copyright 2004 by Susan M. Sigward A Dissertation Presented to the FACULTY OF THE GRADUATE SCHOOL UNIVERSITY OF SOUTHERN CALIFORNIA In Partial Fulfillment of the Requirements for the Degree DOCTOR OF PHILOSOPHY (BIOKINESIOLOGY) August 2004 Susan M. Sigward Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. UMI Number: 3145285 INFORMATION TO USERS The quality of this reproduction is dependent upon the quality of the copy submitted. Broken or indistinct print, colored or poor quality illustrations and photographs, print bleed-through, substandard margins, and improper alignment can adversely affect reproduction. In the unlikely event that the author did not send a complete manuscript and there are missing pages, these will be noted. Also, if unauthorized copyright material had to be removed, a note will indicate the deletion. ® UMI UMI Microform 3145285 Copyright 2004 by ProQuest Information and Learning Company. All rights reserved. This microform edition is protected against unauthorized copying under Title 17, United States Code. ProQuest Information and Learning Company 300 North Zeeb Road P.O. Box 1346 Ann Arbor, Ml 48106-1346 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. DEDICATION This work is dedicated to the Sigward Family and Karen Korytowski. My parents are always there to support me and stand by me proudly no matter what path I choose. My brothers set examples for me by forging their own paths toward happiness and fulfillment in their lives. My nieces make me complete with their love. AND Karen has given me the strength to take this path and has stayed with me through it all with her love and stability. Without her this would not have been possible. Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. ACKNOW LEDGEMENTS This dissertation would not have been possible without the contribution and support of a number of people. I would like to acknowledge the financial support of the Foundation for Physical Therapy and the National Athletic Trainer’s Association whose contributions made this work feasible. Firstly, I would like to acknowledge the contributions of my dissertation committee. While I would like to express my gratitude for the time and assistance provided by my committee, I would also like to recognize the distinct contributions of each member. Foremost, I would like to express my gratitude to Dr. Chris Powers, my academic advisor, who helped develop an idea that I could not even articulate when I arrived into project that I can be proud of. With his mentorship and professionalism he has set a standard of excellence that I only hope to achieve in my career. I would like to thank Dr. George Salem, who served as a source of enduring support and mentorship; Dr. Irene McClay Davis who, more than anyone has contributed to my profession growth by promoting me and my work in the research community; Dr. Jill McNitt-Gray, who challenged my understanding and application of biomechanical principles and Dr. Stan Azen, who has give his time and expertise to this dissertation. I would like to express my appreciation to the over 100 subjects that participated in these studies. The collection and organization of these data would have been unbearable without the assistance of the Susumu Ota, Karen Pelley and Sapna Patel. Special thanks goes to my friend and colleague Susumu Ota, who iii Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. contributed enormously to this dissertation by spending countless hours collecting and processing data, for this I will be forever grateful. Additional thanks go out to members of the USC faculty, who all have contributed to my professional growth and development: Dr. James Gordon and Dr. Sandra Howell provided personal and financial support, and Dr. Kornelia Kulig mentored me on more than one level and provided me with a model for academic excellence. I would be remiss if I were to overlook the assistance of the USC staff, in particular, Jill Hopkins, Gloria Barreras and Janet Cogorno for, among other things, making sure I was always registered and paid on time and Sandra Parra and Sheila Clayborn for their friendship, entertainment and support. Finally, this journey would not have been possible without the love and support of my family, friends and colleagues. My parents, Mike and Nancy Sigward, have always been there to support me in the pursuit of my goals. Karen Korytowski gave me the courage to follow my dreams and the strength to achieve them. All of my colleagues in the lab have become friends and family, in particular, Sam Ward, Matt Sandusky and Kathleen Ganley. Kathleen, your encouragement and understanding have taken me through the tough times. Sam, you have been there from the beginning supporting me, entertaining me and challenging me like no other, thank you. Matt, you have made me look good on several occasions and I know that is not easy. To all my friends from Ohio to Southern California that have propped me up along the way, I am grateful. iv Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. TABLE OF CONTENTS DEDICATION.......................................................................................................................ii ACKNOWLEDGEMENTS..................................................... iii LIST OF TABLES...............................................................................................................vii LIST OF FIGURES............................................................................................................viii ABSTRACT............................................................................................................................ x CHAPTER I:OVERVIEW................................................................................................... 1 CHAPTER II: LITERATURE REVIEW .........................................................................4 The problem of non-contact ACL injuries.................................................................... 4 Mechanisms of non-contact ACL Injuries.....................................................................5 Factors that place females at risk for a non-contact ACL injury................................ 6 Biomechanical Factors.................................................................................................7 Neuromuscular Factors..............................................................................................10 Role of experience in non-contact ACL injuries........................................................ 12 Role of preventative neuromuscular training programs in reducing non-contact ACL injuries.................................................................................................................... 13 Summary.......................................................................................................................... 15 CHAPTER IB: THE INFLUENCE OF GNEDER ON KNEE JOINT KINEMATICS, KINETICS AND MUSCLE ACTIVATION PATTERNS DURING SIDE-STEP CUTTING......................................................................................................17 Introduction......................................................................................................................18 Materials and M ethods....................................................................................................19 Subjects........................................................................................................................19 Instrumentation........................................................................................................... 20 Procedures...................................................................................................................21 Data Analysis.............................................................................................................. 23 Statistical Analysis..................................................................................................... 24 Results.............................................................................................................................. 25 Knee Kinematics.........................................................................................................25 Knee K inetics............................................................................................................. 25 Ground Reaction Forces............................................................................................ 26 Muscle Activation.......................................................................................................26 Discussion........................................................................................................................32 Summary..........................................................................................................................35 v Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER IV: THE INFLUENCE OF EXPEREINCE ON KNEE JOINT KINEMATICS, KINETICS AND MUSCLE ACTIVATION PATTERNS DURING SIDE-STEP CUTTING IN YOUNG FEMALES.......................................................... 36 Introduction.....................................................................................................................37 Materials and Methods...................................................................................................38 Subjects....................................................................................................................... 38 Instrumentation...........................................................................................................39 Procedures...................................................................................................................40 Data Analysis.............................................................................................................. 42 Statistical Analysis..................................................................................................... 43 Results.............................................................................................................................. 44 Kinematics...................................................................................................................44 Kinetics........................................................................................................................ 44 Electromyography...................................................................................................... 45 Discussion........................................................................................................................50 Summary..........................................................................................................................53 CHAPTER V:THE INFLUENCE OF AN INJURY PREVENTION TRAINING PROGRAM ON KNEE KINEMATICS, KINETICS AND MUSCLE ACTIVATION PATTERNS DURING SIDE-STEP CUTTING IN YOUNG FEMALE ATHLETES ................................................................................................................................................54 Introduction..................................................................................................................... 55 Materials and M ethods................................................................................................... 57 Subjects........................................................................................................................57 Instrumentation........................................................................................................... 57 Procedures................................................................................................................... 58 Data Analysis.............................................................................................................. 61 Statistical Analysis..................................................................................................... 63 Results.............................................................................................................................. 63 Kinematics................................................................................................................... 64 Kinetics.........................................................................................................................64 Muscle Activation.......................................................................................................65 D iscussion........................................................................................................................70 Summary..........................................................................................................................72 CHAPTER V I: SUMMARY AND CONCLUSIONS...................................................73 REFERENCES.................................................................................................................... 80 vi Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. LIST OF TABLES Table 3-1. Subject Characteristics..................................................................................20 Table 4-1. Subj ect Characteri sties..................................................................................39 Table 5-1. PEP program exercises................................................................................. 60 Table 5-2. Subject Characteristics..................................................................................63 vii Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. LIST OF FIGURES Figure 2-1. Potential risk factors contributing to ACL injuries in female athletes...............................................................................................................8 Figure 3-1. Comparison of knee joint kinematics between males and females in a) sagittal, b) frontal and c) transverse planes during side-step cutting............................................................................................................. 27 Figure 3-2. Comparison of knee joint moments between males and females in a) sagittal, b) frontal and c) transverse planes during side-step cutting............................................................................................................. 28 Figure 3-3. Comparison of knee net joint moment impulse between the males and females in a) sagittal, b) frontal and c) transverse planes during early deceleration of side-step cutting........................................................ 29 Figure 3-4. Comparison between males and females of a) quadriceps b) medial hamstring and c) lateral hamstring EMG during early deceleration of side-step cutting..................................................................30 Figure 3-5. Comparison between males and females of vertical b) anterior/posterior and c) medial/lateral ground reaction forces during early deceleration of side-step cutting................................ 31 Figure 3-6. Comparison of individual peak frontal plane moments between males and females during early deceleration of side-step cutting..............................................................................................................33 Figure 4-1. Comparison of knee joint kinematics between novice and experienced female athletes in a) sagittal, b) frontal and c) transverse planes during side-step cutting............................................. 45 Figure 4-2. Comparison of knee joint moments between novice and experienced female athletes in a) sagittal, b) frontal and c) transverse planes during side-step cutting..............................................46 Figure 4-3. Comparison of knee net joint moment impulse between the experienced and novice groups in a) sagittal, b) frontal and c) transverse planes during early deceleration of side-step cutting 47 viii Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Figure 4-4. Comparison between novice and experienced female athletes of a) quadriceps b) medial hamstring and c) lateral hamstring EMG during early deceleration of side-step cutting................................. 48 Figure 4-5. Comparison between novice and experienced female athletes of hamstring/quadri cep s co-contraction ratio during early deceleration of side-step cutting................................................................... 50 Figure 4-6. Correlation between the number of years of experience in the sport of soccer and the hamstring to quadriceps co-contraction ratio during early deceleration of side-step cutting.............................................51 Figure 5-1. Comparison of average knee joint kinematics between the intervention and control groups, pre and post season in a) sagittal, b) frontal and c) transverse planes during early deceleration of side-step cutting..................................................................65 Figure 5-2. Comparison of peak knee joint moments between the intervention and control groups, pre and post season in a) sagittal, b) frontal and c) transverse planes during early deceleration of side-step cutting..............................................................................................................66 Figure 5-3. Comparison of knee net joint moment impulse between the intervention and control groups, pre and post season in a) sagittal, b) frontal and c) transverse planes during early deceleration of side-step cutting......................................................................................... 67 Figure 5-4. Comparison of % MVIC between the intervention and control groups, pre and post season in a) medial hamstring, b) lateral hamstring and c) quadriceps EMG during early deceleration of side-step cutting............................................................................................. 68 Figure 6-1. Peak frontal plane moments compared across studies as an index of “at risk” behavior............................................................................77 ix Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. ABSTRACT Biomechanical and neuromuscular risk factors are thought to contribute to the higher incidence of non-contact anterior cruciate ligament (ACL) injuries in female athletes. In addition, it is believed that these risk factors are influenced by experience level and type of training. The objectives of this dissertation were 1) to identify biomechanical and neuromuscular risk factors that may predispose female athletes to non-contact ACL injuries, 2) to evaluate the effects of experience on biomechanical and neuromuscular risk factors, and 3) to assess effectiveness o f a training program in altering lower extremity mechanics. To address these aims, three studies were carried out. Study I compared experienced male (n=15) and female (n=T5) collegiate soccer players, while study II compared novice (n=15) and experienced (n=15) female high school soccer players. Study III evaluated female high-school soccer players (n=20) before and after participating in a 12-week ACL injury prevention program and female high-school soccer players (n=19) not participating in the injury prevention program. Dependent variables analyzed in all three experiments included knee sagittal, frontal, and transverse plane, average kinematics, peak moments, net joint moment impulse, and normalized EMG o f quadriceps and hamstrings during a side-step cutting maneuver. Results from Study I found that during early deceleration, females experienced greater frontal plane moments, smaller sagittal plane moments and greater quadriceps activation than males. Contrary to our original hypothesis, Study II found that novice females demonstrated smaller knee moments and greater muscle co-contraction than experienced females, suggesting a protective x Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. strategy in response to a relatively unfamiliar task. In study III, post-season increases in frontal and transverse plane impulse were seen in the control group and no changes were seen in the group participating in the injury prevention program. Overall, the results of this dissertation provide evidence for the theory that females perform athletic tasks differently than males and suggest that the pattern demonstrated by the females is suggestive of increased risk for ACL injury. Furthermore, it appears that the “at risk” behavior in females increases with athletic experience and participation in an intervention program may act to prevent the emergence of potentially injurious movement patterns. Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER I OVERVIEW Female participation in competitive sports has grown significantly since the passage o f Title IX in 1972. Coincident with this increase has been a disproportionate number of sports related injuries, particularly those involving the anterior cruciate ligament (ACL). Studies comparing injury rates between males and females participating in the same sport have shown a 3-8 times greater incidence of ACL injuries in female athletes.3 ,3 5 ,4 2 Several factors contributing to the gender disparity have been proposed, and typically fall into four categories: hormonal, structural, biomechanical, and neuromuscular. Non-contact ACL injuries have been described as occurring during maneuvers that include deceleration with a change in direction (i.e. landing and cutting tasks). Biomechanical studies evaluating these tasks have identified gender differences in lower extremity kinematics, kinetics and muscle activation patterns. It has been proposed that the patterns demonstrated by females place them at greater risk for ACL injury. However, given that the work in this area is limited with respect to variables analyzed (i.e. kinematics, kinetics and EMG considered separately) a clear understanding of how these biomechanical and neuromuscular differences relate to ACL injury is not known. Gender differences in biomechanical and neuromuscular variables have been attributed to several factors, including sport specific experience. It is thought that 1 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. female athletes, who have little experience in a sport, perform athletic maneuvers in a manner that places them at greater risk of injury. While it is likely that this theory was developed in response to the coincident increases in the availability of sports programs for females and ACL injuries, there is very little evidence to support it. To date, only one study evaluating performance of athletic task as it relates to ACL injury has even considered the influence of experience. The documented success of intervention programs in decreasing ACL injuries in female athletes suggests that training may play a role in injury prevention. However, little is known about the mechanism underlying the success of these programs. While it has been hypothesized that theses injury prevention programs improve performance thereby decreasing injury risk, little work has been done to test this theory. Given the limited work in this area, the objective of this dissertation was to determine the influence of gender, experience and training on ACL injury risk factors. To meet this objective, three studies were undertaken. Each study evaluated the performance of a side-step cutting task as measured by kinematic, kinetic and muscle activation patterns in different populations. Chapter III evaluated male and female college level soccer players to determine if gender differences in biomechanical and neuromuscular variables exist. Chapter IV evaluated novice and experienced female high school soccer players to determine if level o f experience affects biomechanical and neuromuscular risk factors. Finally, Chapter V evaluated female high school soccer players who participated in an ACL injury prevention 2 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. program and compared them to female high school soccer players who did not receive specialized training. SPECIFIC AIMS The principle aims of this dissertation were to: 1. Quantify biomechanical and neuromuscular differences between experienced male and female athletes while performing a side-step cutting maneuver. (Chapter III) 2. Quantify biomechanical and neuromuscular differences between young experienced and novice female athletes while performing a side-step cutting maneuver. (Chapter IV) 3. Assess the influence of an injury prevention program in altering biomechanical and neuromuscular variables of young female athletes during the performance of a side-step cutting maneuver. (Chapter V) Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER II LITERATURE REVIEW THE PROBLEM OF NON-CONTACT ACL INJURIES Female participation in competitive sports has grown significantly since the passage of Title IX in 1972. In the 25-year period following Title IX, participation in sports by high school and collegiate females increased more than 600%.5 0 From 1989 to 1992, the National Collegiate Athletic Association (NCAA) reported a 9% increase in female participants in all athletic programs. The number of institutions supporting women’s soccer increased 48% from 1991 to 1995. Coincident with the increase in female participation in athletic activities, has been a disproportionate number of sports related injuries, particularly those involving the anterior cruciate ligament (ACL). Studies comparing injury rates between males and females participating in the same sport have shown a 3-8 times greater incidence 2 3 35 • • of ACL injuries in female athletes. ’ ’ Assessment of ACL injuries in 893 men’s and women’s NCAA soccer and basketball programs from 1989 to 1993 found the rate of ACL injury per exposure for female athletes was greater than that of their male counterparts. In particular, the rate of ACL injury in female soccer players was 31% as compared to 13% for male soccer players. Similarly, the incidence for female basketball players was found to be 4.1 times greater than for male basketball players.3 Recent figures reported by the National Collegiate Athletic Association (1994-1998) have continued to show a higher incidence of ACL injuries in females.2 This problem, however, is not restricted to collegiate athletes. Comparison of injuries 4 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. of male and female high school basketball players from 1 0 0 schools found that although the overall injury rate per season for males (.56/athlete) was significantly higher than for females (.49/athlete), the risk of ACL injury for females was 3.79 times greater than for males.42 Despite the higher incidence of ACL injury in female athletes, causative mechanisms have not been clearly defined. This is of concern, as an understanding of contributing factors is needed for the development of effective prevention and rehabilitation strategies. To reduce the incidence of non-contact ACL injuries in female athletes, the mechanism of injury (i.e. pathomechanics) and potential risk factors need to be identified. MECHANISM S OF NON-CONTACT ACL INJURIES While an ACL injury can be a result of contact with another player or object, it has been reported that approximately 70% of ACL injuries result from situations that do not involve contact.8,31,41 From a qualitative standpoint, a mechanism of a non-contact ACL injury has been described as occurring just after foot contact, during a maneuver that includes a sharp deceleration and change in direction, with the knee in a position of tibial rotation and valgus and relative knee extension (ie. 1 0 - 3 qo) 8,16 gucj1 m0vements are commonly seen during a forceful cutting maneuver or when landing from a jump. While this injury scenario has been described from data obtained through questionnaires and videotape analysis, 8’31’41 the point at which the ACL fails is unclear. It would appear however, that the mechanism o f injury is Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. related to knee position and combined joint torque that is capable of straining the ACL to the point of failure. The concept of combined loading at the knee as being contributory to ACL injuries is supported by in-vitro studies. Such investigations have shown that a combination of transverse and frontal plane torques at the knee places the greatest stress on the ACL. In particular, it has been found that with the knee positioned between 5° of hyperextension and 40° of flexion, an internal rotation torque combined with a varus or valgus torque will increase the strain on the ACL.1 5 ’ 3 7 This strain is further increased with application of an anterior tibial shear force.3 7 In addition, increased strain due to impingement of the ACL on the intercondylar notch has been demonstrated with combined knee external rotation and valgus.1 9 Although the results of in-vitro studies appear to be consistent with observed mechanisms of ACL injury, objective biomechanical data obtained from athletes (particularly females) while performing sport related maneuvers are limited. It stands to reason that if normal lower extremity kinematic and kinetic during such activities can be described, athletes who demonstrate potentially injurious patterns or “at risk” behavior can be identified. FACTORS THAT PLACE FEMALES AT RISK FOR A NON-CONTACT ACL INJURY Because of the higher incidence of non-contact ACL injuries in female athletes, research attempting to identify risk factors for ACL injury has focused on 6 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. gender differences. In general, gender related risk factors can be grouped into four 25 categories: hormonal, structural, biomechanical, and neuromuscular (Figure 2-1). While hormonal and structural factors are static measures and are relatively fixed for an individual, biomechanical and neuromuscular factors are related to the performance of specific tasks and are more likely amenable to intervention. It stands to reason that investigation of biomechanical and neuromuscular risk factors may be important in assessing the underlying mechanisms of a non-contact ACL injury. Non-Performance Based Risk Factors Performance based Risk Factors Influenced by Experience? Training? ACL Injury (i.e. Poor Muscle Response) Neuromuscular Factors Hormonal (i.e. Kinematics and Kinetics) Biomechanical Factors Structural Figure 2-1. Potential risk factors contributing to ACL injuries in female athletes. Biomechanical Factors Lower Extremity Kinematics Non-contact ACL injuries have been described as occurring during maneuvers that require sudden deceleration and/or a change in direction movement. 7 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. In particular, during a side-step cutting maneuver, subjects land with the knee slightly flexed as they decelerate to a maximal knee flexion angle and then accelerates to push off. At heel strike, the knee internally rotates; peaking with maximal knee flexion, then externally rotates through acceleration.1 1 ,1 3 ,3 4 ,3 9 ,4 0 In the frontal plane, increasing valgus coincides with increasing knee flexion.3 4 ,4 0 Only two studies have compared lower extremity kinematics between males and females during cutting activities.3 4 ,4 0 Malinzak et al.3 4 reported that females demonstrated smaller knee flexion and greater knee valgus angles than males during the stance phase of running, cross cutting and side-step cutting. While McLean et al. 4 0 also found that females maintained slightly greater knee valgus during side step cutting, they found no significant gender differences in sagittal and transverse plane motion. Further evidence in support of gender related differences in lower extremity kinematics has been reported in investigations of single and double limb jumping and squatting tasks. Lephart et al.3 2 found that females landed with greater knee extension, less knee internal rotation and greater hip internal rotation than males. While gender differences have been reported, it should be noted that none of these studies reported kinematic values that suggested the knee was at an end range of motion, indicating that under these experimental conditions, stress on the ACL was likely minimal. 8 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Lower Extremity Kinetics Four studies have investigated lower extremity kinetics during sidestep cutting and landing from a jump,16 ,1 0 ,2 3 and of those, three examined gender differences.1 ,1 0 ,2 4 Besier et al.6 was the first to quantify knee joint moments in male subjects during cutting maneuvers. In regards to side-step cutting, these authors reported that knee flexion and internal rotation moments persisted throughout the cut cycle. Values during the early and late portions of the cut phase were smaller than those observed during the mid-portion of the cycle, where maximal knee flexion occurred. With respect to the frontal plane, a small valgus moment was observed in the early and late portions of stance with a larger varus moment being reported at mid-cycle. However, when analyzing individual frontal plane patterns these authors found that some of the subjects experienced a valgus moment during at the midpoint of the cut cycle. To date, little work has been done to characterize gender differences in knee kinetics during side-step cutting. However, Andriacchi et al.1 examined gender differences in frontal plane hip moments during a 90° side-step cutting task. Male subjects demonstrated a pattern characterized by an initial abduction moment followed by an adduction moment while the females demonstrated a persistent hip adduction moment throughout the cut cycle. Although moments at the knee were not evaluated as a part of this study, the female pattern was found to be associated with 9 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. axial knee joint forces offset from the long axis of the tibia, suggesting that the hip was a possible contributor to excessive or faulty loading of the knee. Evidence in support of gender related differences in knee kinetics has been • 1A 0/1 O 1 reported in studies evaluating jumping and landing activities. ’ Hewett et al. examined landing forces and knee moments during a landing maneuver and found that when compared to males and females demonstrated greater peak vertical landing forces than females. However, no significant differences in sagittal and frontal plane moments at the knee, hip or ankle were reported. In contrast, Chappell and colleagues1 0 reported gender differences in knee kinetics during three stop-jump tasks. When compared to males, females demonstrated greater knee extension and valgus moments during the landing phases of all three activities. To date, a clear understanding of how lower extremity kinematics and kinetics contribute to non-contact ACL injuries in female athletes is lacking. The work in this area has identified gender differences in kinematics and kinetics, but has been limited in scope with respect to variables analyzed (i.e. kinematics and kinetics considered separately). Further evaluation of athletic tasks including kinematic and kinetic variables is necessary for the identification of potentially injurious performance pattern. Neuromuscular Factors While kinematic and kinetic data provide insight into the forces acting at the knee, analysis o f muscle activation patterns is important in determining one’s ability to provide dynamic stability. The quadriceps and hamstrings are considered to 10 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. contribute the greatest muscular support to the knee.3 3 The quadriceps have been found to be an antagonist to the ACL between extension and 50° of flexion.7 ,1 8 On the other hand, the hamstrings are thought to protect the ACL by stabilizing or pulling the tibia posteriorly, thereby resisting anterior translation.7 ,1 8 ’ 4 3 It has been postulated that the hamstrings play a role in preventing excessive tibial rotations due to their insertions on the medial and lateral condyles of the tibia.4 3 Inadequate or inappropriate muscle action may place greater demands on passive structures resulting in injury. Investigations quantifying gender differences in muscle recruitment patterns during athletic maneuvers have focused almost exclusively on the quadriceps and hamstrings. A study assessing muscle activation timing during a side-step cutting maneuver demonstrated that males had longer hamstring and gastrocnemius activation times than females, while females had longer quadriceps activation times than males.3 0 Similarly, females have been reported to demonstrate increased quadriceps activity with decreased hamstring and/or gastrocnemius activity during hoping,5 2 running, crossover cutting and sidestep cutting.3 4 In addition, females have been shown to exhibit preferential quadriceps reflex activation after an imposed anterior tibial perturbation.2 7 This increase in quadriceps activation in females has been described as a “quadriceps dominance” pattern, which has been hypothesized to increase a person’s risk of ACL injury by creating a greater anterior shear of the tibia on the femur.2 7 ,4 4 11 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. To date, gender differences in biomechanical and neuromuscular measure of performance have been identified during activities that are thought to be high risk for ACL injuries, however comprehensive evaluations including lower extremity kinematics, kinetics and muscle activation patterns are lacking. Muscle recruitment patterns of the lower extremity are needed to understand the role of dynamic control in protecting against ACL injury. Biomechanical evaluation of athletic tasks is needed to identify potentially injurious movement pattern. ROLE OF EXPERIENCE IN NON-CONTACT ACL INJURIES Experience level has been proposed as a risk factor in non-contact ACL injuries, suggesting that novice athletes are less equipped to respond to the unfamiliar physical demands of athletic tasks.4 9 In 1978, Garrick et al.2 0 suggested that the majority of female high-school athletes should be considered relative novices and therefore more likely to sustain an injury. This novice status was related to the fact that the 37% of the female, high school athletes had not been participating in their sport for more than two years due to limited access to the sport. Arendt et al.3 speculated that the gender disparity in incidence of ACL injury was due to the rapid increase in the number of available programs for females, thereby, introducing large numbers of less experienced females athletes to the demands of competitive sports. Biomechanical support for the role of experience in contributing to ACL injuries is provided by two studies. Huston and Wojtys et al.2 7 evaluated measures of anterior tibial translation, hamstring strength, quadriceps strength, and reactions to 12 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. anterior tibial perturbation in female athletes and non-athletes and found that athletes had less anterior tibial translation and had greater muscular endurance. Only one study has considered performance differences related to experience level. McLean et al.4 0 investigated the relationship between knee joint kinematics and experience and found a correlation between years of experience and variability in kinematic patterns during side-step cutting. These authors concluded that subjects with fewer years of sport experience were at greater risk of injury due to greater variability in kinematic patterns. To date, no study has comprehensively evaluated the effects of experience level on kinematic, kinetic and EMG variables. Such information is needed to better direct the development and implementation of effective training programs for younger female athletes ROLE OF PREVENTATIVE NEUROMUSCULAR TRAINING PROGRAMS IN REDUCING NON-CONTACT ACL INJURIES It has been hypothesized that the level and type of training are factors that o no on nr* contribute to non-contact ACL injuries. ’ ’ ’ To address the issue of training, several injury prevention programs have been developed. While the exercises and time commitments of each program differ, they generally include elements of o o o o n nr^ endurance, flexibility, strengthening, and proprioception. ’ ’ ’ Studies evaluating the effects of such training programs on incidence of ACL injury have shown promising results. Hewett et al.2 3 prospectively studied the effects of six-week pre- 13 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. season jump training program on incidence knee injuries in female athletes. These authors found that untrained athletes had a 3.6 times higher incidence of injury than trained athletes.2 3 Similarly, Caraffa et al.9 showed that when compared to male soccer players who participated in a proprioceptive training program, untrained athletes had a 7 times greater incidence of ACL tears. Furthermore, a three year study evaluating a soccer specific training program, found that female soccer players participating in the program had an 88% and 74% decrease in the incidence of ACL 36 injury in the first two years, respectively.' The success of these programs strongly suggests that training is a factor in contributing to ACL injuries. Apart from the effectiveness o f intervention studies in reducing ACL injuries, little is known about the mechanism underlying the success of these programs. To date, only one study has attempted to characterize changes in performance following the implementation of a successful ACL injury prevention. Hewett et al.2 4 evaluated lower extremity kinematics and landing forces after participation in a jump-training program. While they found no change in kinematic patterns and average knee joint moments, they did observe a decrease in peak landing forces. Such findings indicate that training may influence biomechanical and neuromuscular aspects of performance. Information regarding performance changes following the implementation of an intervention program that has been found to be successful in reducing the incidence of non-contact ACL injuries may provide insight into the mechanism underlying the success of these programs. Ultimately, 14 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. this information could be useful for designing more effective and efficient injury prevention programs. SUMMARY Epidemiological data has shown that when compared to males, the incidence of non-contact ACL injuries is greater in females. Based on the literature available, it is apparent that the factors that contribute to this discrepancy are not well understood and the mechanism underlying the non-contact ACL tear has not been clearly defined. It is thought that female athletes perform athletic tasks in a manner that places them at greater risk of ACL injury and that novice female athletes perform at a level that places them at even greater risk. While gender differences in biomechanical measures of performance have been evaluated, the work in this area is limited, as kinematics, kinetics, and muscle activity have been studied separately. Furthermore, little information exists regarding the effects of previous experience in a sport on biomechanical and neuromuscular variables. The success of various intervention programs suggests that changes in performance may influence injury incidence. However, as a result of varied exercise regimens and subject populations, it is difficult, if not impossible to determine what type of training is most appropriate and what subject population is in need of training. Comprehensive evaluations of sport specific activities (i.e. lower extremity kinematics, kinetics, and muscle activity) are needed to answer key questions related to gender, age, and training. 15 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. These issues are important in furthering our understanding and prevention of ACL injuries in female athletes. Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER in THE INFLUENCE OF GENDER ON KNEE KINEM ATICS, KINETICS AND M USCLE ACTIVATION PATTERNS DURING SIDE-STEP CUTTING It has been suggested that gender differences in the performance of athletic maneuvers is a contributory factor with respect to the disproportionate incidence of non-contact ACL injury in female athletes. Previous work evaluating gender differences in performance is limited as aspects of kinematics, kinetics, and muscle activation patterns have been studied separately. This chapter compared gender differences in knee joint kinematics, kinetics and muscle activation during a side step cutting maneuver in thirty healthy college level soccer players (15 male, 15 female). Data were analyzed to determine if females perform this maneuver differently than their male counterparts, and if females perform this task in a manner that is suggestive of increased risk of ACL injury. 17 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. INTRODUCTION Studies comparing injury rates between males and females participating in the same sport have shown a greater incidence of ACL injuries in female athletes.3 ,3 5 ,4 2 For example, assessment of ACL injuries in 893 men’s and women’s NCAA soccer and basketball programs from 1989 to 1993 found the rate of ACL injury per exposure for female athletes was greater than that of their male counterparts (2.8 and 4.1 times respectively). Recent figures reported by the National Collegiate Athletic Association (1994-1998) have shown that this trend is continuing.2 While an ACL injury can be a result of contact with another player or object, it has been reported that approximately 70% of ACL injuries result from situations that do not involve contact.8 ,1 1 ,4 1 From a qualitative standpoint, the mechanism of a non-contact ACL injury has been described as occurring just after foot contact during a maneuver that includes a sharp deceleration and change in direction.8 At this point, the knee has been described to be in a position o f internal rotation, valgus, and relative extension (i.e. 0-30°).3 1 Data from in vitro studies appear to be consistent with observed mechanisms of ACL injury demonstrating that the ACL is I r 'i'- ] o o loaded in these positions. ’ ’ To date, several studies have attempted to identify gender related differences in performance that may predispose females to ACL injuries. With respect to kinematics, females have been found to demonstrate greater knee valgus3 4 ,4 0 and smaller knee flexion angles than males during cutting.3 4 In addition, evaluation of 18 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. muscle activation patterns using electromyography (EMG) has revealed that females demonstrate greater quadriceps and less hamstring activity than males during cutting.3 4 While these studies have provided important information about gender differences during sport specific tasks, a comprehensive evaluation of knee joint kinematics, kinetics and muscle activation patterns has not been performed. Given that the torque at the knee is likely an important aspect of the mechanism of ACL injury, such a study is needed to better understand injurious movement patterns that could put females at greater risk. The purpose of this study was to evaluate gender differences in knee joint kinematics, kinetics, ground reaction forces and muscle activation during side-step cutting. Based on previous literature in this area it was hypothesized that when compared to males, females would demonstrate: 1) reduced knee flexion and greater knee valgus, 2) greater frontal and transverse plane moments at the knee and 3) increased activation of the quadriceps and decreased activation of the hamstrings. Information from this study will be useful in determining if females perform this maneuver differently than their male counterparts and if they perform it in a manner that is suggestive of increased risk for ACL injury. MATERIALS AND METHODS Subjects Thirty soccer players (15 male and 15 female) between the ages o f 18 and 27, participated in this study (Table 1). Subjects were NCAA Division I or II athletes 19 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. with at least 1 year of collegiate experience. The average years of soccer experience for the females and males in this study was 13.4 + 2.2 yrs. and 12.4 + 3.0 yrs., respectively. All subjects were healthy with no current complaints of lower extremity injury. Subjects were excluded from the study if they reported any of the following: 1) hi story of previous ACL injury or repair 2) previous injury that resulted in ligamentous laxity at the ankle, hip or knee or, 3) presence of any medical or neurologic condition that would impair their ability to perform a side-step cutting task. Table 3-1 Age (yrs) Height (cm) Weight (kg) Years of experience Males (n=15) 19.7 ± 2.2 179.1+6.0* 74.2 ± 7.0* 12.4 ± 3.0 Females (n=15) 19.4 ± 1.5 167.4 ±8.0 65.9 ± 7 .0 13.4 ±2.2 Subject Characteristics Means + sd * indicates males greater than females (p < 0.05). Instrumentation Three-dimensional motion analysis was performed using a computer aided video (Vicon) motion analysis system (Oxford Metrics LTD. Oxford, England). Kinematic data were sampled at 120 Hz and recorded digitally on dual Pentium III 1GHz personal computer. Reflective markers (25 mm spheres) placed on specific 20 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. boney landmarks (see below) where used to calculate motion of the pelvis, hip, knee and ankle in the sagittal, frontal and transverse planes. Ground reaction forces where collected at a rate of 2400 Hz using an AMTI force plate (Model#OR6-6-1, Newton, MA). EMG activity of the vastus lateralis and of the medial and lateral hamstring muscles were recorded at 2400 Hz, using pre-amplified bipolar, surface electrodes (Motion Control, Salt Lake City, UT). EMG signals were telemetered to a 12-bit analog to digital converter using an FM- FM telemetry unit. Differential amplifiers were used to reject the common noise and amplify the remaining signal (gain=1000). Procedures All testing took place at the Musculoskeletal Biomechanics Research Laboratory at the University of Southern California. Prior to participation, all procedures were explained to each subject and informed consent was obtained as approved by the Institutional Review Board for the University o f Southern California Health Sciences Campus. Prior to testing, each subjects’ skin was shaved and cleaned with alcohol. Surface EMG electrodes were then placed over the quadriceps (vastus lateralis), lateral hamstrings (biceps femoris) and medial hamstrings (semimebranosis and semitendinosis) of the right leg in accordance with procedures described by Cram et al. 1 2 Electrodes were secured with tape and an elastic sleeve. The EMG telemetry unit was worn in a pack secured to the subject’s back. 21 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. To allow for comparison of EMG intensity between subjects and muscles, and to control for variability induced by electrode placement, EMG obtained during the cutting maneuver was normalized to the EMG acquired during a maximal voluntary isometric contraction (MVIC). The MVIC test for the quadriceps was performed with the subject seated (hip and knee flexed to 90° and 60°, respectively), and pushing against a fixed resistance. The MVIC for the medial and lateral hamstrings was performed in supine with the hip and knee flexed to 30°. A strap was secured to the table and placed around the subject’s hips which allowed them to perform a single leg bridge (i.e. resisting hip extension with the knee flexed). Each MVIC was held for six seconds. Following the MVIC’s, reflective markers were placed on the following anatomical landmarks: bilateral anterior superior iliac spines, posterior superior iliac spines, lateral epicondyles of the knee, lateral malleoli, calcaneus, and bases of the fifth metatarsal.2 9 The thigh and calf markers were mounted on 5 cm wands and secured on the thigh and shank with elastic bands. The foot markers were placed on the shoes. To control for the potential influence of varying footwear, subjects were fitted with same style of cross-training shoe (New Balance Inc., Boston, MA). Each participant performed four trials of a side-step cutting maneuver. Subjects were instructed to run five meters at a speed of 5.5-7.0 m/s before contacting their right foot on the force plate and then change direction to the left at an angle between 35-60° from the original direction of motion. Approach speed was calculated with the use of a photoelectric switch and force plate contact. The trial 22 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. was considered acceptable if the subject landed on the force plate at the pre determined speed. Practice trials allowed the subjects to become familiar with the procedures and instrumentation. D ata Analysis Vicon Clinical Manager (VCM) software (Oxford Metrics LTD. Oxford, England) was used to quantify lower extremity motion and moments in the sagittal, frontal and transverse planes. Kinematic data was filtered using a Woltering quintic spline filter with a predicted mean square error of 20 mm. Net joint moments were calculated with standard inverse dynamics equations. Net joint moment impulse was calculated as the integral of the net joint moment over time. To facilitate comparison of moment data between groups, all kinetic data were normalized to body mass. Raw EMG data was filtered with a band pass Butterworth filter (20-500 Hz) with a roll off of 5 and a 60 Hz notch filter. Full wave rectification and smoothing of the EMG signal was accomplished using root-mean-square (RMS) values over a 75 ms interval. The processed EMG signal from each MVIC trial was averaged over 1- second intervals, with the greatest 1-second average being used for normalization purposes. EMG collected from the cutting trials were expressed as a percentage of the EMG obtained during MVIC (% MVIC). All data were normalized to 100% of the cut cycle. The cut cycle was identified as the period from initial contact of the right foot to toe off, as determined 23 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. by the force plate recordings. For the purposes of this study, only the early deceleration phase of the cutting cycle was considered as this is the time in which the majority of non-contact ACL injuries have been reported to occur.8 Early deceleration was defined as the first 20% of the cut cycle; the time in which the knee o is in less than 40° of flexion. The dependent variables evaluated in this study included the following: average knee motion during early deceleration (sagittal, frontal and transverse plane); peak knee moments during early deceleration (sagittal, frontal and transverse plane); net knee joint moment impulse during early deceleration (sagittal, frontal and transverse plane); peak ground reaction forces during early deceleration (vertical, medial/lateral and anterior/posterior);and average EMG (quadriceps, medial and lateral hamstrings) during early deceleration. For each subject, all dependent variables represented the mean of the four trials collected. Statistical Analysis To determine if average knee kinematics, peak knee moments, net joint moment impulse, peak ground reaction forces, and average EMG differed between genders, one-tailed, independent samples t-tests were performed. Statistical analyses were performed using SPSS statistical software (Chicago, IL). Significance levels where set at p< 0.05. 24 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. RESULTS Knee Kinematics There were no significant differences in average sagittal plane knee kinematics between males and females during early deceleration (p=0.18; Figure 3- la). This finding also was consistent for the frontal and transverse planes (p= 0.14 and 0.12, respectively; Figure 3-lb-c). Knee Kinetics During early deceleration, males demonstrated a significantly greater peak knee flexor moment than females (2.1 + 0.84 vs. 1.4 + 0.77 Nm/kg; p=0.025; Figure 3-2a). On average, females demonstrated a greater initial peak adductor moment (valgus) than males (-0.43 + 0.5 vs. 0.006 + 0.3 Nm/kg; p= 0.005; Figure 3-2b). In regards to peak transverse plane moments, there were no significant differences found between males and females (p=0.4; Figure 3-2c). When compared to female athletes, male athletes demonstrated larger sagittal plane net joint moment impulse at the knee during early deceleration (0.06 ± 0.02 vs. 0.042 + 0.02 Nmsec/kg; p=0.009; Figure 3-3a). No significant differences were found in the net joint moment impulse in the frontal and transverse planes (p= 0.18 and 0.26, respectively; Figure 3b-c). 25 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Ground Reaction Forces During early deceleration females demonstrated a significantly greater peak medial ground reaction force (10.2 + 3.07 vs. 8.6 + 1.81 N/Kg; p=0.04; Figure 3-5c). There were no significant differences in peak lateral, anterior, posterior or vertical, ground reaction forces (p= 0.09, 0.15, 0.41 and 0.43, respectively; Figure 3-5a-b). Muscle Activation During early deceleration, female subjects demonstrated greater average quadriceps EMG than males (191 vs. 151% MVIC, p=0.02; Figure 3-4a) There were no significant differences in average EMG of the medial or lateral hamstrings (p= 0.17 and 0.07, respectively; Figure 3-4b-c). 26 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. a) Sagittal - - Male — Female 0 10 20 30 40 50 60 70 80 90 100 % Cut Cycle b) Frontal 40 ■ - M ale — Fem ale 20 30 -20 - " O X ! -40 % Cut Cycle c) Transverse 30 - • M ale — Fem ale 20 % Cut Cycle Figure 3-1. Comparison of knee joint kinematics between males and females in a) sagittal, b) frontal and c) transverse planes during side-step cutting. Vertical dashed line indicates end o f early deceleration phase. No group differences were observed. Error bars equal 1 standard deviation. Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. a) Sagittal © e 0 ) -w W in O s C P ! O X ) a z 4 3 2 1 0 - - M ale — Fem ale -1 •2 -3 % Cut Cycle b) Frontal ■ • M ale — Female 1.5 -a 0.5 T T T u J -1.5 % Cut Cycle c) Transverse ■ a a © > * C P W 1 W D a E « Z + - > a 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0 - 0.1 - 0.2 - M ale Fem ale i0 30 40 50 60 70 80 8 % Cut Cycle Figure 3-2. Comparison of knee joint moments between males and females in a) sagittal, b) frontal and c) transverse planes during side-step cutting. Vertical dashed line indicates end o f early deceleration phase. * indicates significant gender differences (p < 0.05). Error bars equal 1 standard deviation. Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. a) Sagittal * 0.08 0.06 o 0.04 C M S 0.02 0 Fem ales M ales O 4 ) CM 0.06 $ 0.04 S 0.02 Z 0 b) Frontal Fem ales M ales 0.006 $ 0.004 ~ < D 4 J I 0.002 2 ; 0 c) Transverse Fem ales M ales Figure 3-3. Comparison of knee net joint moment impulse between the males and females in a) sagittal, b) frontal and c) transverse planes during early deceleration of side-step cutting * indicates males >females (p < 0.05). Error bars equal 1 standard deviation. Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. a) Quadriceps 250 200 150 % 100 50 0 o> Fem ales M ales b) Medial Hamstrings Fem ales M ales c) Lateral Hamstrings Fem ales M ales Figure 3-4. Comparison between males and females of a) quadriceps b) medial hamstring and c) lateral hamstring EMG during early deceleration of side-step cutting. * indicates females > males (p < 0.05). Error bars equal 1 standard deviation. Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. a) Vertical 100 ||S f - 2 0 Fem ale % Cut Cycle b) Anterior/Posterior ■ ■ M ale — Fem ale -5 6 10 io 30 40 50 60 70 80 90 100 % Cut Cycle c) Medial/Lateral J « I) fjjO 2j0 30 40 50 60 70 8^ 5 < S • - < u 0 i P Q 1 8J3 -5 IS ■ o £ S 10 15 '0 100 • ■ M ale — Fem ale % Cut Cycle Figure 3-5. Comparison between males and females of a) vertical b) anterior/posterior and c) medial/lateral ground reaction forces during early deceleration of side-step cutting. * indicates females > males (p < 0.05). Error bars equal 1 standard deviation. Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. DISCUSSION The results of this study found that gender differences exist while performing a side-step cutting maneuver. More specifically, females demonstrated smaller sagittal plane moments and greater frontal plane moments than males during early deceleration. Additionally, when compared to males, females exhibited greater quadriceps activation. Surprisingly, no gender differences in knee kinematics were observed. With respect to knee kinetics, females demonstrated an average adductor (valgus) moment during early deceleration, whereas the male subjects demonstrated an average abductor (varus) moment (Figure 3-2b). Although gender differences were evident in peak frontal plane moments, the net joint moment impulse did not differ between groups. These data indicate that while there were no differences in overall load on the joint in the frontal plane, females demonstrated a different torque at the knee than their male counterparts (i.e. valgus vs. varus). The gender differences in peak frontal plane knee moments become more apparent when the individual data were plotted in ascending order. As shown in Figure 3-6, 80% of the females demonstrated an adductor (valgus) moment compared to only 40% of the males. On average, the females demonstrated peak frontal moments that were 2 times greater than their male counterparts. We feel that this finding is important as in vitro and modeling studies have found that an abductor (valgus) torque can increase the load on the ACL,4 ,3 7 ,3 8 particularly at small knee flexion angles.3 7 ,3 8 The fact that this gender difference occurred during early 32 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. deceleration of the cut cycle when the knee is in minimum knee flexion (i.e. < 40°) could be interpreted as “at risk” behavior. Peak Frontal Plane Moments Male F em ale Figure 3-6. Comparison o f individual peak frontal plane moments between males and females during early deceleration of side-step cutting. Each bar represents an individual subject One possible explanation for the greater adductor moments demonstrated by the female athletes could be the presence of greater frontal plane shear forces. The only significant difference in ground reaction forces during early deceleration was seen in the medial/lateral direction. The female athletes demonstrated greater medial ground reaction forces (Figure 3-5c) which coincided with a knee abductor moment. While it was not significant females demonstrated a trend toward larger lateral ground reaction forces (p=0.09) which coincided with the peak valgus moment during early deceleration. The lack of significant differences in lateral ground reaction forces may be attributed to the analysis o f average data, as not all females demonstrated large adductor moments. Further investigation o f individual GRF data is warranted. Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. With regards to peak sagittal plane moments, all subjects demonstrated a net knee flexor moment during early deceleration. However, the female athletes demonstrated a significantly smaller peak flexor moment and net joint moment impulse than the male athletes. This finding may be explained by the muscle activation pattern exhibited by the females during this phase. As the knee flexor moment represents the net joint moment in the sagittal plane (the sum of the flexor and extensor moments), the observed increase in knee extensor activity in the females could have resulted in an increase in the extensor moment, and in turn, a reduction of the net flexor moment. Our EMG results support the findings of Malinzak et al.3 4 who reported that females demonstrated increased quadriceps activity compared to males during a side step cutting task. However, these authors also noted decreased hamstring activity in their female subjects. In contrast, our data found no significant gender differences in hamstring activation, and if anything, females tended to have greater hamstring activity than the males suggesting increased co-contraction about the knee. Given that quadriceps force has been shown to increase strain in the ACL by increasing anterior tibial shear7 ’1 4 ,1 5 ,1 7 ’ 3 8 ’ 4 5 ’ 4 8 and hamstring force have been shown to decrease this strain,7 ,4 5 it is unclear if this muscle activation pattern would place the females at greater risk of ACL injury. No gender differences were observed in the sagittal, transverse or frontal plane knee kinematics. This finding was surprising as previous studies have reported gender differences in knee sagittal and frontal plane angles using similar side-step 34 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. cutting procedures. For example, females have been found to have smaller knee flexion3 4 and greater knee valgus angles4 0 than males. It should be noted, however, that these studies evaluated recreational athletes and skilled athletes with varying years of experience. The population in this study was comprised of college level soccer players with a combined average of 12.9 + 2.6 years of experience. The fact that the current study did not find gender differences in kinematic patterns may be attributed to a more skilled, homogenous population. SUMMARY The results of this study provide evidence in support of the theory that females perform certain athletic maneuvers in a way that may predispose them to ACL injury. However, it should be noted that evaluation of individual data suggests that only a percentage of females may be considered “at risk” as some females demonstrated kinematic, kinetic and muscle activation patterns that were similar to that of males. In addition, since this study only evaluated high level collegiate athletes, an argument could be made that females who have successfully participated in high risk sports (such as soccer) for an extended period of time may represent a group of women who have found appropriate adaptive measures. Whether or not similar biomechanical patterns during side-step cutting would be evident in younger, less-skilled, populations remains to be seen. 35 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER IV THE INFLUENCE OF EXPERIENCE ON KNEE JO IN T KINEM ATICS, KINETICS AND MUSCLE ACTIVATION PATTERNS DURING SIDE-STEP CUTTING IN YOUNG FEMALE ATHLETES It is thought that female athletes with limited experience in a sport perform athletic maneuvers differently than their more experienced counterparts, and that they do so in a manner that places them at greater risk for injury. However, there is little evidence to support this premise. To evaluate the influence of experience on biomechanical and neuromuscular variables, this chapter compared knee joint kinematics, kinetics and muscle activation patterns during a side-step cut between novice (n=15) and experienced (n=15) female high school soccer players. 36 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. INTRODUCTION Female participation in competitive sports has grown significantly since the passage of Title IX in 1972. Coincident with this increase in participation, has been a disproportionate number of sports related injuries, particularly those involving the anterior cruciate ligament (ACL). Studies comparing injury rates between male and female athletes participating in the same sport have shown a 3-8 times greater incidence of ACL injuries in female athletes.3’ 3 5 ,4 2 Despite the higher incidence of ACL injury in females, causative mechanisms have not been clearly defined. This is of concern, as an understanding of contributing factors is needed for the development of effective preventative strategies. Athletic experience is one factor thought to place females at risk for ACL injury. It has been suggested that novice athletes are less equipped to respond to the unfamiliar physical demands of athletic tasks,4 9 and that the rapid increase in the number of available programs for females has introduced large numbers o f less experienced females athletes to the demands o f competitive sports.3 Although research attempting to identify risk factors for ACL injury has focused on differences between males and females,1 0 ’ 3 2 ’34’ 4 0 few have explored the role of experience as a contributing risk factor. To date, only two studies have evaluated the effects of experience on the potential for ACL injury. Huston et al. (1996)2 7 found that when compared to female athletes, non-athletic females demonstrated decreased muscular endurance and increased anterior tibial translation. McLean et al., 19994 0 suggested that 37 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. athletes with fewer years of sport experience may be at greater risk for ACL injury due to more variable kinematic patterns at the knee during side-step cutting. Although such studies point to experience as being a potential risk factor with respect to ACL injuries, more comprehensive investigations comparing novice and experienced athletes are needed. In particular, no study has evaluated the influence of experience on knee kinetics during sports activities. Given the limited work in this area, the purpose of this study was to evaluate the influence of experience on knee joint kinematics, kinetics and muscle activation patterns during the execution of a side-step cutting maneuver in female athletes and to determine if when compared to experienced females, novice females exhibit behavior that is suggestive of greater risk of ACL injury. Based on the previous literature related to proposed mechanisms of non-contact ACL injuries it was hypothesized that when compared to experienced female athletes, novice female athletes would demonstrate: 1) reduced knee flexion and greater knee valgus, 2) greater frontal and transverse plane moments at the knee and 3) increased activation of the quadriceps and decreased activation of the hamstrings. MATERIALS AND METHODS Subjects Thirty healthy females between the ages of 14 and 16 participated in this study (Table 1). Fifteen of the subjects had 8 or more years of experience playing soccer (10.8 + 1.4 years on average) and were classified as experienced, while fifteen 38 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. of the subjects had 5 or less years of experience playing soccer (2.0 + 1.5 years on average) and were classified as novice. All subjects were recruited from local club soccer teams and area high schools. All subjects were healthy with no current complaints of lower extremity injury. Subjects were excluded from the study if they reported any of the following: 1) history of previous ACL injury or repair 2) previous injury that resulted in ligamentous laxity at the ankle, hip or knee or, 3) presence of any medical or neurologic condition that would impair their ability to perform a side-step cutting task. Table 4-1 Subject Characteristics Mean + sd Height (cm) Weight (kg) Age (yrs) Novice 157.9 + 5.9 58.8 + 9.4 15.4 + 1 (n=15) Experienced 164.4 ± 4.3* 56.7 ±7.5 15.4 ± 1 (n=15) * experienced group significantly greater than novice group Instrumentation Three-dimensional motion analysis was performed using a computer aided video (Vicon) motion analysis system (Oxford Metrics LTD. Oxford, England). Kinematic data were sampled at 120 Hz and recorded digitally on dual Pentium III 1GHz personal computer. Reflective markers (25 mm spheres) placed on specific Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. boney landmarks (see below) where used to calculate motion of the pelvis, hip, knee and ankle in the sagittal, frontal and transverse planes. Ground reaction forces where collected at a rate of 2400 Hz using an AMTI force plate (Model#OR6-6-l, Newton, MA). Electromyographic activity o f the vastus lateralis and of the medial and lateral hamstring muscles were recorded at 2400 Hz, using pre-amplified bipolar, surface electrodes (Motion Control, Salt Lake City, UT). EMG signals were telemetered to a 12-bit analog to digital converter using an FM-FM telemetry unit. Differential amplifiers were used to reject the common noise and amplify the remaining signal (gain=1000). Procedures All testing took place at the Musculoskeletal Biomechanics Research Laboratory at the University o f Southern California. Prior to participation, all procedures were explained to each subject and informed consent was obtained as approved by the Institutional Review Board for the University o f Southern California Health Sciences Campus. Prior to testing, each subjects’ skin was shaved and cleaned with alcohol. Surface EMG electrodes were then placed over the quadriceps (vastus lateralis), lateral hamstrings (biceps femoris) and medial hamstrings (semimebranosis and semitendinosis) of the right leg in accordance with procedures described by Cram et al.1 2 Electrodes were secured with tape and an elastic sleeve. The EMG telemetry unit was worn in a pack secured to the subject’s back. 40 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. To allow for comparison of EMG intensity between subjects and muscles, and to control for variability induced by electrode placement, EMG obtained during the cutting maneuver was normalized to the EMG acquired during a maximal voluntary isometric contraction (MVIC). The MVIC test for the quadriceps was performed with the subject seated (hip and knee flexed to 90° and 60°, respectively), and pushing against a fixed resistance. The MVIC for the medial and lateral hamstrings was performed in supine with the hip and knee flexed to 30°. A strap was secured to the table and placed around the subject’s hips which allowed them to perform a single leg bridge (i.e. resisting hip extension with the knee flexed). Each MVIC was held for six seconds. Following the MVIC’s, reflective markers were placed on the following anatomical landmarks: bilateral anterior superior iliac spines, posterior superior iliac spines, lateral epicondyles of the knee, lateral malleoli, calcaneus, and bases of the fifth metatarsal2 9 The thigh and calf markers were mounted on 5 cm wands and secured on the thigh and shank with elastic bands. The foot markers were placed on the shoes. To control for the potential influence of varying footwear, subjects were fitted with same style of cross-training shoe (New Balance Inc., Boston, MA). Each participant performed four trials of a side-step cutting maneuver. Subjects were instructed to run five meters at a speed of 5.5-7.0 m/s before contacting their right foot on the force plate and then change direction to the left at an angle between 35-60° from the original direction of motion. Approach speed was calculated with the use of a photoelectric switch and force plate contact. The trial 41 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. was considered acceptable if the subject landed on the force plate at the pre determined speed. Practice trials allowed the subjects to become familiar with the procedures and instrumentation. D ata Analysis Vicon Clinical Manager (VCM) software (Oxford Metrics LTD. Oxford, England) was used to quantify lower extremity motion and moments in the sagittal, frontal and transverse planes. Kinematic data was filtered using a Woltering quintic spline filter with a predicted mean square error of 20 mm. Net joint moments were calculated with standard inverse dynamics equations. Net joint moment impulse was calculated as the integral of the net joint moment over time. To facilitate comparison of moment data between groups, all data kinetic were normalized to body mass. Raw EMG data was filtered with a band pass Butterworth filter (20-500 Hz) with a roll off of 5 and a 60 Hz notch filter. Full wave rectification and smoothing of the EMG signal was accomplished using root-mean-square (RMS) values over a 75 ms interval. The processed EMG signal from each MVIC trial was averaged over 1- second intervals, with the greatest 1-second average being used for normalization purposes. EMG collected from the cutting trials were expressed as a percentage of the EMG obtained during MVIC (% MVIC). All data were normalized to 100% of the cut cycle. The cut cycle was identified as the period from initial contact of the right foot to toe off, as determined 42 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. by the force plate recordings. For the purposes of this study, only the early deceleration phase of the cutting cycle was considered as this is the time in which the majority of non-contact ACL injuries have been reported to occur.8 Early deceleration was defined as the first 20% of the cut cycle; the time in which the knee is in less than 40° of flexion.8 The dependent variables evaluated in this study included the following: average knee motion during early deceleration (sagittal, frontal and transverse plane); peak knee moments during early deceleration (sagittal, frontal and transverse plane); net knee joint moment impulse during early deceleration sagittal, frontal and transverse plane); and average EMG (quadriceps, medial and lateral hamstrings) during early deceleration. For each subject, all dependent variables represented the mean of the four trials collected. Statistical Analysis To determine if average knee kinematics, peak knee moments, net joint moment impulse and average EMG differed between groups, one-tailed, independent samples t-tests were performed. Statistical analyses were performed using SPSS statistical software (Chicago, IL). Significance levels where set at p< 0.05. 43 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. RESULTS Kinematics There were no significant differences in sagittal plane knee kinematics between novice and experienced females during early deceleration (p= 0.73; Figure 4-la). This finding was consistent for the frontal and transverse planes (p= 0.26 and 0.17, respectively; Figure 4-lb-c). Kinetics During early deceleration, novice athletes demonstrated smaller knee flexor moments (0.1 + 1.3 vs. 1.2 ± 0.6 Nm/kg; p= 0.003; Figure 4-2a), smaller peak knee adductor (valgus) moments (0.4 + 0.5 vs. 0.9 + 0.6 Nm/kg; p= 0.01; Figure 4-2b), and smaller peak knee internal rotator moments (0.08 + 0.07 vs. 0.18 + 0.1 Nm/kg; p= 0.005; Figure 4-2c) than experienced athletes. Similarly, novice athletes demonstrated smaller sagittal, frontal and transverse plane net joint moment impulse at the knee during early deceleration when compared to experienced athletes (0.03 + 0.01 vs. 0.04 + .02 Nmsec/kg; p=0.04; 0.02 ± 0.008 vs. 0.03 + 0.008 Nmsec/kg; p=0.005 and 0.003 + 0.001 vs. 0.004 + 0.002 Nmsec/kg; p=0.002, respectively; Figures 4-3 a-c). Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Electromyography There were no significant differences between novice and experienced females in average quadriceps, medial hamstring or lateral hamstring EMG during early deceleration (p= 0.42, 0.17, and 0.4, respectively; Figures 4-4 a-c). Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. e « « 5 5 C J •g £ 4 0 J If 3 0 T 3 w 2 0 a) Sagittal Novice Experienced 10 20 30 40 50 60 70 80 90 100 % Cut Cycle b) Frontal Novice Experienced „ U l i l U l U l i t o m f n i i i H i i 1 ■5-10 i) 100 % Cut Cycle c) Transverse M $ 0 Novice Experienced liiiiiniiiiii % Cut Cycle Figure 4-1. Comparison of knee joint kinematics between novice and experienced female athletes in a) sagittal, b) frontal and c) transverse planes during side-step cutting. Vertical dashed line indicates end of early deceleration phase. No group differences were observed. Error bars equal 1 standard deviation. Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 0960 a) Sagittal s * © tf i s < u -M * & o n . S o Z « e u 4 — Novice ■ ■ Experienced 3 2 1 0 1 -2 % Cut Cycle b) Frontal © H 3 £ s z " O T3 < Novice Experienced 30 40 50 60 70 80 90 100 % Cut Cycle c) Transverse Novice ■ Experienced I P io 30 40 50 60 70 80 9<Tl00 % Cut Cycle Figure 4-2. Comparison of knee joint moments between novice and experienced female athletes in a) sagittal, b) frontal and c) transverse planes during side-step cutting. Vertical dashed line indicates end of early deceleration phase. * indicates novice group < experienced group (p < 0.05). Error bars equal 1 standard deviation. 47 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 02 a) Sagittal g 0.04 Z 0.02 a Experienced Novice b) Frontal Experienced Novice D D 5 0 s £ 0.008 0.006 0.004 0.002 c) Transverse Experienced Novice Figure 4-3. Comparison of knee net joint moment impulse between the experienced and novice groups in a) sagittal, b) frontal and c) transverse planes during early deceleration of side-step cutting * indicates novice group < experienced group (p < 0.05). Error bars equal 1 standard deviation. Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. a) Quadriceps 300 - 250 - u ) * H Experienced N ovice b) Medial Hamstrings 1 0 0 -i 80 - Experienced N ovice c) Lateral Hamstrings 100 -| 80 - Experienced N ovice Figure 4-4. Comparison between novice and experienced female athletes of a) quadriceps b) medial hamstring and c) lateral hamstring EMG during early deceleration of side-step cutting. No group differences were observed. Error bars equal 1 standard deviation. Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. DISCUSSION The results of this study found that differences exist between novice and experienced female athletes during the early deceleration phase of a side-step cutting maneuver. More specifically, novice females demonstrated smaller peak knee flexor, adductor, and internal rotator moments than their experienced counterparts. In addition novice females demonstrated smaller net joint moment impulse in the transverse and frontal planes. The disparity in knee kinetics between groups was evident in the absence of kinematic differences, suggesting that the experienced and novice females employed different neuromuscular control strategies to complete the cutting task. The lower peak moments and net joint moment impulse in the novice group would not appear to place them at risk for ACL injury as modeling and in vitro studies have shown an increased load in the ACL with larger frontal and transverse plane torques applied to the knee.1 5 ’1 9 ’ 3 7 The larger peak transverse and frontal plane moments and impulse demonstrated by the experienced female athletes would suggest that this group was exposed to larger moments for a longer duration than novice athletes. This would appear to place more experienced athletes at greater risk for ACL injury, which is contrary to our original hypothesis. Despite the fact that there were no differences in the average EMG amplitude of the individual muscle groups, one possible explanation for the decreased moments at the knee in the novice group may have been the presence of greater co-contraction. To further explore this issue, a co-contraction ratio was calculated during early 50 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. deceleration using the methods described by Besier et al. 2003.5 Briefly, the ratio of flexor to extensor activation was calculated by dividing the average activation of flexors (medial and lateral hamstrings) by the average activation of extensors (vastus lateralis). A ratio of 1 would be indicative of pure co-contraction. This post-hoc analysis showed that novice females had a significantly greater co-contraction ratio than experienced females when analyzed using an independent samples t-test (0.44 + Co-contraction Ratio 0.75 - 0.5 J 0.25 J 0 - E x p erienced N ovice Figure 4-5. Comparison between novice and experienced female athletes of hamstring/quadriceps co-contraction ratio during early deceleration of side-step cutting * indicates novice > experienced group (p < 0.05). Error bars equal 1 standard deviation. 0.2 vs. 0.34 + 0.1; p=0.04; Figure 4-5). Furthermore, a post-hoc Pearson’s correlation analysis found a negative relationship between the number of years of experience and the co-contraction ratio (r=-0.32; p=0.04; Figure 4-6), suggesting that as females with greater amounts of experience perform the cutting task with less knee co-contraction. 51 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Taken together, our results suggest that the novice athletes may adopt a protective strategy of muscle co-contraction in response to a relatively novel task. With experience, a pattern of reduced co-contraction and greater knee moments appears to emerge. These results are consistent with the principles of skill acquisition, where the initial response to a novel task (i.e. mass co-contraction) is progressively refined by repression of unnecessary muscular activity into an efficient movement strategy.4 7 ’ 5 1 Reduced co-contraction and the emergence of greater knee moments in more experienced female athletes suggest that these individuals have developed a more specific movement strategy with greater exposure to the task. ♦ ♦ ♦ ❖ « ► ♦ ♦ r= -0.32 0 0.2 0.4 0.6 0.8 1 Co-contraction Ratio Figure 4-6. Correlation between the number of years of experience in the sport of soccer and the hamstring to quadriceps co-contraction ratio during early deceleration of side-step cutting. p=0.04 52 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. SUMMARY The results of this study demonstrate that novice and experienced female athletes employ different neuromuscular control strategies while performing a side step cutting maneuver. While the kinetic patterns demonstrated by the more experienced females are consistent with the pattern of skill acquisition, they are also more suggestive of an “at risk” pattern for ACL injury. This suggests that females may be more susceptible to injury as they gain experience and confidence in this task. Future work is needed to test this hypothesis and to determine what factors contribute to the development of these strategies, as this information could be used to direct the development and implementation of effective training programs. 53 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER V THE INFLUENCE OF AN ACL INJURY PREVENTION TRAINING PROGRAM ON KNEE KINEMATICS, KINETICS AND MUSCLE ACTIVATION PATTERNS DURING SIDE-STEP CUTTING IN YOUNG FEMALE ATHLETES Although several injury prevention programs have been found to reduce the incidence of ACL injuries in female athletes, little is known about the mechanism underlying their success. This chapter evaluated the influence of an ACL injury prevention program knee joint kinematics, kinetics and muscle activation patterns female high school athletes (n=20) compared to a control group of female high school athletes (n=T9), who did not participate in the injury prevention program. Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. INTRODUCTION Anterior cruciate ligament (ACL) injuries are commonly sustained by individuals who engage in athletics. Approximately 70% of these injuries occur during activities that do not involve contact with another player or object such as cutting or landing from a jump.8 ,3 1 ,4 1 Female athletes have been shown to have a 3-8 times greater incidence of non-contact ACL injuries than their male counterparts. It has been hypothesized that females employ movement patterns and/or neuromuscular control strategies that may predispose them to non-contact ACL injuries.2 1 ,2 8 ,4 9 For example, biomechanical and neuromuscular studies evaluating potentially injurious cutting maneuvers have identified gender related differences in knee joint kinematics and muscle activation patterns.3 4 ,4 0 Several factors have been thought to contribute to gender related differences in performance including, decreased joint proprioception,2 1 ,4 6 diminished strength,2 7 ,4 9 poor conditioning,2 6 ,4 9 altered neuromuscular control strategies,2 1 and inadequate training. To address the issue of training in female athletes, several injury prevention programs have been developed. While the exercises and time commitments of each program differ, they generally include elements of endurance, flexibility, 9 22 23 24 36 strengthening, and proprioception. ’ ’ ’ ’ Studies evaluating the effects o f such training programs on the incidence of ACL injury have shown promising results. A prospective study evaluating the effects of a jump training program on incidence of serious knee injuries in female athletes found that untrained athletes had a 3.6 times higher incidence of injury than the trained athletes.2 3 A study of gradually increasing 55 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. proprioceptive training in 600 male soccer players showed that untrained athletes had a 7 times greater incidence of ACL tears.9 More recently, a two-year prospective study evaluating female soccer players who participated in a sport specific training program found the incidence of non-contact ACL injury in this population to be 74% less than that of players who did not participate in the program.3 6 Apart from the apparent effectiveness of these interventions in reducing ACL injuries, little is known about the mechanism underlying the success of such programs. To date, only one study has evaluated changes in lower extremity mechanics following the implementation of a jump training program.2 4 Although this investigation found no changes in lower extremity kinematics following training, a decrease in peak landing forces was observed.2 4 While such findings suggest that training can influence biomechanical aspects of performance, more work is needed to better understand the effects of these programs on decreasing risk for ACL injury. Given the limited work in this area, the purpose of this study was to evaluate the effects of an intervention program that has been shown to decrease the incidence of ACL injury on knee joint kinematics, kinetics and muscle activation patterns during side-step cutting. It was hypothesized that following the intervention, female athletes would demonstrate patterns that would be suggestive of decreased risk for ACL injury including: 1) increased knee flexion and reduced knee valgus, 2) reduced frontal and transverse plane moments at the knee and 3) increased activation of the hamstrings with decreased activation of the quadriceps. 56 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. MATERIALS AND METHODS Subjects Fifty-seven female soccer players between the ages of 14 and 17 were initially contacted to participate in this study. Subjects were recruited from five area club and high school soccer teams. All subjects were healthy with no current complaints of lower extremity injury. Subjects were excluded from the study if they reported any of the following: 1) history of previous ACL injury or repair 2) previous injury that resulted in ligamentous laxity at the ankle, hip or knee or, 3) presence of any medical or neurologic condition that would impair their ability to perform a side-step cutting task. O f the five teams contacted to participate in this study, three of the teams agreed to participate in the intervention program. Therefore, the subjects were not randomly assigned to groups and a quasi-experimental pretest-posttest design with a control group was used. Subjects in the training group (n= 33) participated in a 10 week ACL injury prevention program as part of their normal soccer practice (see below). The subjects in the control group (n=24) participated in their normal soccer practice and did not receive the injury prevention program. Instrumentation Three-dimensional motion analysis was performed using a computer aided video (Vicon) motion analysis system (Oxford Metrics LTD. Oxford, England). Kinematic data were sampled at 120 Hz and recorded digitally on dual Pentium III 57 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 1GHz personal computer. Reflective markers (25 mm spheres) placed on specific boney landmarks (see below) where used to calculate motion of the pelvis, hip, knee and ankle in the sagittal, frontal and transverse planes. Ground reaction forces where collected at a rate of 2400 Hz using an AMTI force plate (Model#OR6-6-l, Newton, MA). Electrical activity o f the vastus lateralis and of the medial and lateral hamstring muscles were recorded at 2400 Hz, using pre-amplified bipolar, surface electrodes (Motion Control, Salt Lake City, UT). EMG signals were telemetered to a 12-bit analog to digital converter using an EM- FM telemetry unit. Differential amplifiers were used to reject the common noise and amplify the remaining signal (gain=1000). Procedures Each subject participated in two testing sessions, one at the beginning of the soccer season and one following the soccer season. All testing took place at the Musculoskeletal Biomechanics Research Laboratory at the University of Southern California. Prior to participation, all procedures were explained to each subject and informed consent was obtained as approved by the Institutional Review Board for the University of Southern California Health Sciences Campus. Prior to testing, each subjects’ skin was shaved and cleaned with alcohol. Surface EMG electrodes were then placed over the quadriceps (vastus lateralis), lateral hamstrings (biceps femoris) and medial hamstrings (semimebranosis and semitendinosis) of the right leg in accordance with procedures described by Cram et 58 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. al.1 2 Electrodes were secured with tape and an elastic sleeve. The EMG telemetry unit was worn in a pack secured to the subject’s back. To allow for comparison of EMG intensity between subjects and muscles, and to control for variability induced by electrode placement, EMG obtained during the cutting maneuver was normalized to the EMG acquired during a maximal voluntary isometric contraction (MVIC). The MVIC test for the quadriceps was performed with the subject seated (hip and knee flexed to 90° and 60°, respectively), and pushing against a fixed resistance. The MVIC for the medial and lateral hamstrings was performed in supine with the hip and knee flexed to 30°. A strap was secured to the table and placed around the subject’s hips which provided resistance while they performed a single leg bridge (i.e. hip extension with the knee flexed). Each MVIC was held for six seconds. Following the MVIC’s, reflective markers were placed on the following anatomical landmarks: bilateral anterior superior iliac spines, posterior superior iliac spines, lateral epicondyles of the knee, lateral malleoli, calcaneus, and bases of the fifth metatarsal.2 9 The thigh and calf markers were mounted on 5 cm wands and secured on the thigh and shank with elastic bands. The foot markers were placed on the shoes. To control for the potential influence of varying footwear, subjects were fitted with same style of cross-training shoe (New Balance Inc., Boston, MA). Each participant performed four trials of a side-step cutting maneuver. Subjects were instructed to run five meters at a speed of 5.5-7.0 m/s before contacting their right foot on the force plate and then change direction to the left at 59 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. an angle between 35-60° from the original direction of motion. Approach speed was calculated with the use of a photoelectric switch and force plate contact. The trial was considered acceptable if the subject landed on the force plate at the pre determined speed. Practice trials allowed the subjects to become familiar with the procedures and instrumentation. Following the initial biomechanical assessment, subjects in the training group participated in the “Prevent injury and Enhance Performance” (PEP) exercise program developed by the Santa Monica Orthopaedic and Sport Medicine Research Foundation (Santa Monica, CA). Prior to the study, each coach received written and video-taped instructions on proper implementation the PEP program. Briefly, the program took 15-20 minutes and consisted of a pre-determined series of warm-up, stretching, strengthening, plyometrics, and sport specific agility drills (Table 5-1). The coaches were instructed to emphasize correct posture, straight up and down jumps without excessive side-to-side movement, and to reinforce soft landings. The program was performed 2-3 times a week during the season and was monitored by the coach to ensure adherence and proper technique. Two site visits were made during the season by one of the investigators to ensure proper implementation o f the program. Subjects in the control group participated in their regular soccer practice 2-3 times a week for the duration of the soccer season (approximately 10 weeks). Following completion of the soccer season, all subjects returned to the 60 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Musculoskeletal Biomechanics Research Laboratory where they underwent a post season biomechanical assessment using the identical procedures as described above. Table 5-1. PEP program exercises 1. Warm-up: (30-60 seconds each) A. Jog line to line B. Shuttle Run C. Backward Running 2. Stretching: (30 sec x 2 reps) A. Calf stretch B. Quadriceps stretch C. Figure Four Hamstring stretch D. Inner Thigh Stretch E. Hip Flexor Stretch 3. Strengthening: (30 reps x 2 reps) A. Walking Lunges B. Russian Hamstring C. Single Toe Raises 4. Plyometrics: (20 reps) A. Lateral Hops over Cone B. Forward/Backward Hops over cone C. Single Leg hops over cone D. Vertical Jumps with headers E. Scissors Jump 5. Agilities A. Shuttle run with forward/backward running B. Diagonal runs C. Bounding run Data Analysis Vicon Clinical Manager (VCM) software (Oxford Metrics LTD. Oxford, England) was used to quantify lower extremity motion and moments in the sagittal, frontal and transverse planes. Kinematic data was filtered using a Woltering quintic spline filter with a predicted mean square error of 20 mm. Net joint moments were calculated with standard inverse dynamics equations. Net joint moment impulse was 61 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. calculated as the integral of the net joint moment over time. To facilitate comparison of moment data between groups, all kinetic data were normalized to body mass. Raw EMG data was filtered with a band pass Butterworth filter (20-500 Hz) with a roll off of 5 and a 60 Hz notch filter. Full wave rectification and smoothing of the EMG signal was accomplished using root-mean-square (RMS) values over a 75 ms interval. The processed EMG signal from each MVIC trial was averaged over 1- second intervals, with the greatest 1-second average being used for normalization purposes. EMG collected from the cutting trials were expressed as a percentage of the EMG obtained during MVIC (% MVIC). All data were normalized to 100% of the cut cycle. The cut cycle was identified as the period from initial contact of the right foot to toe off, as determined by the force plate recordings. For the purposes of this study, only the early deceleration phase of the cutting cycle was considered as this is the time in which the majority of non-contact ACL injuries have been reported to occur.8 Early deceleration was defined as the first 20% of the cut cycle; the time in which the knee is in less than 40° of flexion.8 The dependent variables evaluated in this study included the following: average knee motion (sagittal, frontal and transverse plane); peak knee moments (sagittal, frontal and transverse plane); net knee joint moment impulse (sagittal, frontal and transverse plane) and average EMG (quadriceps, medial and lateral 62 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. hamstrings) during early deceleration. For each subject, all dependent variables represented the mean of four trials collected Statistical Analysis To determine if average knee kinematics, peak knee joint moments, net joint moment impulse and average EMG differed between groups (training vs. control) over time (pre season vs. post season), 2 X 2 ANOVA’s with repeated measures on one variable (time) were performed. This analysis was performed for each dependent variable. In the event of a significant interaction, post-hoc testing was performed. Statistical analyses were performed using SPSS statistical software (Chicago, IT). Significance levels where set at p< 0.05. RESULTS During the course of the study, 18 subjects were lost to attrition (5 in the control group, 13 in the training group). In the control group, two subjects did not return due to injury (ankle sprain and knee tendonitis), and three subjects were lost to follow-up. In regards to the intervention group, four subjects withdrew from the study following injury or illness not related to sport, two subjects were lost to follow- up, and the data for seven subjects were not considered as it was determined that the coach did not implement the program throughout the entire season. Therefore, the following data represents the remaining 39 subjects (training group, n=20, control group, n=19) (Table 5-2). 63 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Table 5-2 Subject Characteristics Mean + sd Height (cm) Weight (kg) Age (yrs) Training group 162.2 ± 6.7 58.8 ±9.6 15.0 ± 1 (n= 20) Control group 161.6 + 5.8 57.3+6.7 15.9+ .9* (n=19) * indicates control group greater than training group Kinematics There were no significant differences in average sagittal plane knee kinematics between groups during early deceleration (no group x time interaction; p=0.21; Figure 5-la). This finding was consistent for both the frontal and transverse planes (no group x time interaction; p=0.45 and 0.59, respectively; Figure 5-lb-c). Kinetics There were no significant differences in peak knee sagittal plane moments between groups during early deceleration (no group x time interaction; p= 0.91; Figure 5-2a). This finding was consistent for both the frontal and transverse planes (no group x time interaction; p= 0.29 and p=0.14, respectively; Figure 5-2 b-c). There was a significant group x time interaction (p=0.032) for net knee joint moment impulse in the frontal plane. Post-hoc analysis revealed that the control group demonstrated an increase in the knee frontal plane net joint moment impulse post season (0.024 ± 0.009 vs. 0.029 ± 0.01 Nmsec/kg; p=0.02; Figure 5-3b). 64 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Subjects in the training group showed no change in the knee frontal plane impulse between sessions. In regard the transverse plane, there also was a significant group x time interaction (p=0.05) for knee transverse plane net joint moment impulse. Similar to the results found in the frontal plane, the control group demonstrated an increase in knee transverse plane net joint moment impulse post season when compared to pre season values (0.0029 + 0.001 vs. 0.0037 + 0.001 Nmsec/kg; p=0.03; Figure 5-3c). Subjects in the training group showed no change in the knee transverse plane impulse between sessions. Although there was a significant group x time interaction for net joint moment impulse in the sagittal plane (p=0.34) post-hoc analysis revealed no difference in sagittal plane net joint moment impulse post season in control or training group (p=0.061 and 0.28, respectively). Muscle Activation There were no significant differences in average quadriceps activation between groups during early deceleration (no group x time interaction; p=0.87; Figure 5-4a). This finding was consistent for both medial and lateral hamstring activation (no group x time interaction; p=0.80 and 0.81, respectively; Figure 5-4 b- c). 65 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. a) Sagittal Training Control b) Frontal 6 n * A S 3 4 - T T U -6 J Training Control c) Transverse 30 - i | 25 - Training Control H p re season H post season Figure 5-1. Comparison of average knee joint kinematics between the training and control groups, pre and post season in a) sagittal, b) frontal and c) transverse planes during early deceleration of side-step cutting. No significant differences were observed. Error bars equal 1 standard deviation Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. £ 5 - » O ' X 4 ) s © © tm S C M c u, © - w c 3 2.5 2 1.5 1 0.5 0 2 1.5 % m & 2 M o 1 3 M 1 T 5 W 3 1 ^ 1 0.5 0 0.8 0.6 - & 0.4 ' ^ I 0.2 0 a) Sagittal Training Control b) Frontal Training Control c) Transverse Training Control H p re season B post season Figure 5-2. Comparison of peak knee joint moments between the training and control groups, pre and post season in a) sagittal, b) frontal and c) transverse planes during early deceleration o f side step cutting. No significant differences were observed. Error bars equal 1 standard deviation Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. £ < y s z 0.07 n 0.06 - 0.05 - 0.04 J 0.03 - 0.02 - 0.01 - 0 - a) Sagittal 0.006 0.005 $ 0.004 0.003 0.002 0.001 0 o v se s z T rain in g Control b) Frontal 2 0.02 Z 0.01 T rain in g Control c) Transverse T rain in g Control I pre season H post season Figure 5-3. Comparison o f knee net joint moment impulse between the training and control groups, pre and post season in a) sagittal, b) frontal and c) transverse planes during early deceleration of side step cutting * indicates significant differences between pre season and post season testing, (p < 0.05) Error bars equal 1 standard deviation 68 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. 300 n 250 - u 200 - | 150 - ^ 100 - 50 - 0 J a) Quadriceps a'' 100 75 50 25 0 150 U 100 I 50 0 Training Control b) M edial Ham strings Training Control c) Lateral H am strings T raining Control II pre season m post season Figure 5-4. Comparison of % MVIC between the training and control groups, pre and post season in a) quadriceps b) medial hamstring, and c) lateral hamstring EMG during early deceleration of side-step cutting. No significant differences were observed. Error bars equal 1 standard deviation Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. DISCUSSION Inadequate training has been theorized to be a risk factor with respect to ACL injuries in female athletes. Given as such, various training programs have been developed to address this issue. While several of these programs have been found to be successful in decreasing the incidence of ACL injury in the female athlete,23’ 3 6 the mechanism behind their success is not clear. We sought to determine if one particular training program would result in changes in biomechanical and neuromuscular variables that would be suggestive of decreased risk for ACL injury. Our initial hypothesis stated that following training, female athletes would demonstrate kinematic, kinetic and muscle activation patterns that would be suggestive of decreased risk of ACL injury. This hypothesis was not supported in that the group participating in the intervention program did not demonstrate changes in the variables evaluated. Instead, the control group demonstrated changes in knee kinetics that could be interpreted as being more indicative of “at risk” behavior. Although the control group did not demonstrate differences in knee joint kinematics or peak knee moments, significant increases in the net joint moment impulse were observed. The net joint moment impulse is the area under the moment curve and represents the overall torque experienced at the knee over a period of time (i.e. early deceleration). On average, the control group demonstrated a 17.5 % and 19.0 % increase in knee frontal and transverse plane impulse respectively, indicating that the overall torque at the knee in these planes was greater post season. The trend toward increased moments in the control group could be interpreted as “at risk” 70 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. behavior as in-vitro and modeling studies have found that frontal and transverse plane torques increase the load on the ACL, particularly when the knee is in relative extension (i.e. 0-40 of knee flexion)4 ’1 5 ,3 7 ,3 8 As the control group did not receive any specialized training during their season, the presence of post season changes could be attributed to participation in a season of soccer (i.e. increased experience). The increase in the frontal and transverse plane knee impulse in the control group is consistent with the results of Chapter IV, This study identified a pattern of reduced co-contraction and the emergence o f greater knee moments as females gain athletic experience. As increases in frontal and transverse plane impulse seen in the control group may be indicative of greater risk of ACL injury, these data suggest that the intervention program may work to suppress the emergence of potentially injurious kinetic patterns at the knee in the young female athlete. Care must be taken in generalizing the results of this study to females of all ages as only young adolescent athletes were evaluated. It is possible that the influence of training may differ among athletes of different age and skill level. For example, it is not known if a young female experiencing pubertal changes (i.e. height, weight, and body composition) would respond differently to a specific training program than one who was older or younger. In addition, it is not known how athletes of varying skill levels respond to training programs. For example, implementation of a training program in a more experienced population (ie. collegiate athletes) may have produced changes not evident in the current study. 71 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. The results of this study could have been affected by several methodological limitations. For example, a relatively small sample size was studied as a result of a high drop out rate (31%). In addition, there were only a limited number of coaches willing to implement the program as a part of their practice, and therefore, subjects were not randomized to experimental and control groups. Additionally, compliance was difficult to assess, as daily administration of the programs was dependent on the coaches. SUMMARY Following an additional season o f soccer experience, young female athletes demonstrated increases in knee frontal and transverse plane impulse while athletes who participated in an ACL injury prevention program did not exhibit changes in knee joint moments. Together these results suggest that injury prevention programs may work to reduce ACL injuries through suppression of potentially injurious behavior patterns in young female athletes. 72 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. CHAPTER VI: SUMMARY AND CONCLUSIONS To address the issue of higher incidence of non-contact ACL injuries in female athletes, this dissertation focused on answering questions related to biomechanical and neuromuscular risk factors related to the performance of a sport specific task. In particular, three studies were designed to gain insight into the influence of gender, experience and training on the performance of a side-step cutting maneuver. It was hypothesized that differences would be seen between males and females and between novice and experienced female athletes and that these differences would indicate that females, and in particular novice females, are at greater risk for ACL injury. Furthermore, it was hypothesized that participation in an injury prevention program would alter biomechanical and neuromuscular patterns that would be suggestive of decreased risk for injury. For each of the above investigations, athletes who had participated in the sport of soccer were studied. The early deceleration phase of side-step cutting was analyzed, as this is the time in which the majority of non-contact ACL injuries have been reported to occur.8 In addition, this phase of the cut cycle is a time when the ACL is thought to be more susceptible to applied torques due to the position of relative knee extension (<40° of flexion).3 7 ,3 8 For each study, biomechanical (knee joint kinematics and kinetics) and neuromuscular (muscle activation patterns) variables were compared between groups. 73 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. As female athletes have been shown to have a greater incidence of non- contact ACL injury than their male counterparts, it has been proposed that females perform athletic maneuvers differently than males and that they do it in a manner that places them at greater risk of ACL injury. The purpose of Chapter III was to evaluate differences in performance between male and female college level soccer players. The results of this study supported the theory that females perform athletic maneuvers differently than males in that they revealed gender differences in knee moments and muscle activation patterns. Furthermore, these differences provided evidence to support the premise that females perform cutting maneuvers in a manner that may predispose them to non-contact ACL injuries. During early deceleration, females demonstrated an average adductor (valgus) moment, whereas the male subjects demonstrated an average abductor (varus) moment. This difference was most apparent when individual data was evaluated 80% of the female athletes demonstrated a peak adductor (valgus) moment during early deceleration, compared to only 40% of the male subjects. This is could be interpreted as “at risk” behavior as in vitro and modeling studies have found that at small knee flexion angles, frontal and transverse plane torques can increase the load on the ACL.4 ’ 3 7 ’ 3 8 Gender differences where also seen in sagittal plane moments and muscle activation patterns. Female athletes demonstrated a significantly smaller peak flexor moment and net joint moment impulse than the males indicating that they generated smaller knee flexor moments throughout early deceleration. In addition, female 74 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. athletes demonstrated greater quadriceps muscle activation than the males. While it is unclear how these sagittal plane gender differences relate to risk of ACL injury, previously published data suggests that a greater flexor moment would be more ACL protective.7 ,1 0 ’1 4 ,1 5 ,1 8 ’ 3 4 ,3 8 ’ 4 5 ’ 4 8 More specifically, these studies have shown that isolated quadriceps force can increase the strain on the ACL through anterior tibial i 7,14,15,18,38.45,48 shear. To date, information regarding gender differences in performance o f athletic tasks has been limited to kinematic and EMG analyses. This study was the first to include a comprehensive evaluation of kinematics, kinetics and EMG, and the results strengthen the theory that males and females perform athletic maneuvers differently. Furthermore, it can be argued that the kinetic and EMG patterns demonstrated by the female athletes place them at greater risk of injury. However, evaluation of individual data suggests that perhaps only a percentage of females may be considered “at risk” as some females demonstrated kinematic, kinetic and muscle activation patterns that were similar to that of males. Gender differences in performance of sport specific activities have been attributed to several factors (i.e. strength, lower extremity alignment, experience) however, research linking these factors and ACL injury mechanisms are limited. With regard to experience, it is thought that female athletes who have little experience in a sport perform athletic maneuvers differently than their more experienced counterparts and that they do so in a manner that places them at greater risk of injury. The purpose of Chapter IV was to evaluate the effect of experience on 75 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. the performance of side-step cutting in novice and experienced high-school soccer players. The results of this study found differences in knee joint moments between the two groups suggesting that the amount of experience in a sport can influence the performance of a sport specific task however, the results of this study did not support the hypothesis that novice females perform athletic maneuvers in a manner that place them at greater risk of ACL injury. The novice females evaluated in Chapter IV, demonstrated smaller peak knee flexor, adductor, and internal rotator moments; and smaller transverse and frontal plane net joint moment impulse than the more experienced females. While no differences in average EMG were found between groups, the novice females demonstrated greater quadricep s/hamstring co-contraction than their experienced counterparts. This increased co-contraction provides a possible explanation for the decreased moments seen in the novice group. As noted above, modeling and in-vitro studies show that the larger transverse and frontal plane moments place greater strain on the ACL.1 5 ,1 9 ,3 8 Contrary to our original hypothesis, these data suggest that the experienced female athletes may be at greater risk for ACL injury than novice athletes. The pattern demonstrated by the novice females (i.e. greater knee co contraction and smaller knee moments) is consistent with that of an unskilled movement. On the other hand, the pattern of frontal and sagittal plane moments demonstrated by the experienced females in this study was similar to that o f the college level females in Chapter III. Taken together these data suggest that with 76 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. experience some female athletes develop a strategy of task execution that may place them at greater risk of injury. The influence of experience on performance in male athletes is not known, however the pattern demonstrated by the college level males in Chapter III suggests males may develop a different kinetic pattern with experience. The documented success of intervention programs in decreasing ACL injuries in female athletes suggests that training may play a role in injury prevention. The purpose of Chapter V was to evaluate the influence of training on the performance of a side-step cutting maneuver in female high school soccer players. Biomechanical and neuromuscular variables were obtained before and after implementation of an injury prevention program and were compared to a control group who did not participate in the training program. While no changes were found in the group participating in the intervention program, the control group demonstrated changes in knee joint kinetics. The 17.5 % and 19.0 % increase in knee frontal and transverse plane net joint moment impulse, respectively, indicates that the overall load on the knee in these planes was greater in the control group post season. As increases in frontal and transverse plane impulse may be indicative of greater risk of ACL injury, these data suggest that the intervention program may work to suppress the emergence of potentially injurious kinetic patterns. A consistent finding across all three studies in this dissertation was differences in frontal plane knee kinetics. For example, differences were found between males and females, novice and experienced females, and following a year of 77 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. soccer experience without training. If one considers increased knee frontal plane moments, especially valgus moments, as being a risk factor for ACL injury, interesting trends are observed (Figure 6-1). For example, it is evident that collegiate male athletes demonstrated the lowest peak frontal plane moments during early deceleration across studies. The male collegiate athletes were followed by the young novice and trained females, who demonstrate lower frontal plane moments than the collegiate female athletes. The two groups who had the greatest frontal plane knee moments were the young experienced and untrained females. These two groups demonstrated knee valgus moments that were almost two times greater than the other groups evaluated. The trends in frontal plane moments at the knee suggest that experience and training may influence “at risk” behavior. Young Females (Experienced)____________________________ (Untrained)________________________ Collegiate Females Young Females jg iiiiilllliliiiiiii Collegiate Males i---------------------- ------------------------1 --------------------~ i---------------------- 1 -----------------------1 -----------------------1 -0 1 2 0 0 l 2 ft4 ft6 0.8 1 Adductor Nm/Kg-Bwt Figure 6-1. Peak frontal plane moments during early deceleration of side step cutting. Comparisons across studies as an index of “at risk” behavior. 78 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. Taken together, the results of this dissertation show that collegiate male and female athletes demonstrate different kinetic and muscle control strategies during a side-step cutting maneuver. Furthermore, the strategy demonstrated by a large proportion of the female athletes may be suggestive of “at risk” behavior for ACL injury. Athletic experience appears to contribute to the development of movement strategies in young female athletes and the implementation of injury prevention programs may be most effective early on, as the female athlete gains experience in a sport, to prevent the development of these patterns. 79 Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. REFERENCES 1. Andriacchi,T., Carmarillo,D., Alexander,E., Dyrby,C. and Huston,L.J.: Gender differences in the biomechanics of running and cutting maneuvers relative to non-contact ACL injury. Proceedings of the 47th Annual Meeting, Orthopaedic Research Society, San Francisco, CA., 07972001. 2. Arendt E, Agel J, Dick R. Anterior cruciate ligament injury patterns among collegiate men and women. Journal o f A thletic Training. 1999;34:86-92. 3. Arendt E, Dick R. Knee injury patterns among men and women in collegiate basketball and soccer. NCAA data and review of literature. 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Creator Sigward, Susan M. (author)

Core Title Biomechanical and neuromuscular aspects of non-contact ACL injuries: The influence of gender, experience and training

School Graduate School

Degree Doctor of Philosophy

Degree Program Biokinesiology

Publisher University of Southern California (original), University of Southern California. Libraries (digital)

Tag health sciences, recreation,health sciences, rehabilitation and therapy,OAI-PMH Harvest

Language English

Contributor Digitized by ProQuest (provenance)

Advisor Powers, Christopher (committee chair), Azen, Stanley (committee member), Davis, Irene M. (committee member), McNitt-Gray, Jill (committee member), Salem, George (committee member)

Permanent Link (DOI) https://doi.org/10.25549/usctheses-c16-417711

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