DISTEFANO, LINDSAY J.; CASA, DOUGLAS J.; VANSUMEREN, MEGAN M.; KARSLO, RACHEL M.; HUGGINS, ROBERT A.; DEMARTINI, JULIE K.; STEARNS, REBECCA L.; ARMSTRONG, LAWRENCE E.; MARESH, CARL M.
Lower extremity musculoskeletal injuries due to sport and physical activity are extremely common and costly (13,24). Besides being associated with great financial costs, these injuries are also associated with devastating long-term consequences, such as the early development of osteoarthritis (15). These consequences demonstrate the need for effective injury prevention. The first step toward effective lower extremity injury prevention is identifying and understanding the risk factors for injury.
Measures of neuromuscular control, such as poor balance (17) and movement technique (12), during sport-specific tasks have been identified as factors that influence the risk of lower extremity injury, such as injuries to the anterior cruciate ligament (ACL). Although balance and movement technique can be considered primary risk factors for lower extremity injury, there may be other issues that influence these primary risk factors in an individual. For example, individuals’ lower extremity movement patterns change under the influence of fatigue (2). Failing to address possible secondary risk factors for injury could limit the long-term effects of injury prevention.
Hypohydration, hyperthermia, and fatigue are frequently present during physical activity participation and may impair neuromuscular control. Hypohydration elevates internal body temperature, which can predispose an individual to hyperthermia (1). An increase in body temperature due to exercise stress reduces optimal function of the central nervous system (10), which may impair judgment and body awareness, resulting in lower extremity injury. Although we are not aware of any studies that have evaluated the effects of hyperthermia or hypohydration on lower extremity movement technique, several studies have investigated the influence of hypohydration on postural control ability (3,8,14,25) with inconclusive results. These studies may have been confounded by the additional influence of fatigue or hyperthermia resulting from the exercise protocol used to induce hypohydration, which limits understanding hypohydration’s influence on postural control.
Several studies have reported higher incidences of injury late in games or practice sessions (11,26), which suggests that fatigue may be a significant risk factor for injury. Previous research demonstrates that both movement technique (2,18) and postural control (7,20) are negatively affected after strenuous exercise sessions. Similar to the studies evaluating hypohydration and postural control, many of these studies may have simultaneously induced hypohydration and/or hyperthermia in addition to fatigue, which makes understanding the role of fatigue on postural control and other measures of neuromuscular control difficult.
Hypohydration, hyperthermia, and fatigue interact during exercise. However, few studies have successfully isolated the effects of these interactions on postural and neuromuscular control, which limits our ability to develop interventions to alleviate these adverse outcomes. Therefore, the purpose of this study was to identify the individual and combined influences of hypohydration, hyperthermia, and fatigue after exercise on lower extremity movement technique and postural control. We hypothesized that hypohydration, hyperthermia, and fatigue after exercise would all result in postural control and movement technique deficits.
Participants completed four test sessions in a randomized order. Each test session was separated by at least 72 h to allow participants to recover from the previous session. The test sessions varied based on the environmental conditions and the participants’ hydration status: euhydrated temperate (EUT), euhydrated hot (EUH), hypohydrated temperate (HYT), and hypohydrated hot (HYH). Temperate and hot conditions were performed in 18.0°C ± 0.2°C, 50.0% ± 3.5% relative humidity, and 34°C ± 0.3°C, 45.0% ± 4.5% relative humidity, respectively. All test sessions took place in a climate-controlled chamber (model 2000; Minus-Eleven Inc., Malden, MA).
Twelve healthy unacclimatized aerobically trained adult men between the ages of 18 and 39 yr volunteered for this study (age = 20 ± 2 yr, height = 182 ± 8 cm, mass = 74.0 ± 8.2 kg, body fat = 8.8% ± 2.8%, range = 5.3%–12.4%, V˙O2max = 57.0 ± 6.0 mL·kg−1·min−1; mean ± SD). All participants reported participating in at least 6 h of moderate exercise per week and a minimum V˙O2max of 50 mL·kg−1·min−1. Participants were excluded if they had any chronic health problems; a history of cardiovascular, metabolic, or respiratory disease; fever; or other current illness or injury that would limit physical activity at the time of testing. Participants were also excluded if they had previously experienced exertional heatstroke or heat exhaustion within the past 3 yr or were on a diet (restricted calories) at time of the study. All participants provided informed consent, and the study was approved by the university’s institutional review board before completing any test or familiarization sessions.
Before the four test sessions, participants attended two familiarization sessions to allow them to become acquainted with the test chamber, the equipment they would be wearing (rectal thermometer and HR monitor), the exercise protocol, the movement technique, and the postural control assessments. All participants were instructed on the insertion of a rectal thermometer (YSI 401 rectal probe, Yellow Spring, OH) for the purposes of monitoring rectal temperature (Tre) throughout the exercise sessions.
During the first familiarization session, participants performed a V˙O2max test to ensure they met the inclusion criteria. Subjects were weighed to the nearest 0.1 kg before the familiarization sessions using a calibrated scale (Health o meter, model 349KLX; Pelstar, Bridgeview, IL). After completing 30 min of walking on the treadmill (1.34–1.78 m·s−1 5% grade), participants were weighed again to determine the sweat rate via body mass (BM) change. Participants wore a standard 20.45-kg rucksack while they walked on a treadmill to increase the difficulty of the exercise protocol and to replicate the standard pack commonly issued in military scenarios. To ensure euhydration before the familiarization sessions, subjects were asked to consume 500 mL of fluid before going to sleep the night before and during waking. Hydration status was measured on arrival to the laboratory via urine specific gravity (Usg ≤ 1.020) (refractometer, model A300CL; Atago Inc., Spartan, Tokyo, Japan), urine color (Ucol ≤ 4) via urine color chart, and urine osmolality (UOsm ≤ 800) (freezing point depression, model 3320; Advanced Instruments, Norwood, MA). Subjects were instructed on the use of the thirst sensation, thermal sensation, and RPE scales. During the second familiarization session, percent body fat was calculated (Lange Skinfold Caliper; Beta Technology Inc., Santa Cruz, CA). Finally, participants also practiced the movement and postural control assessment protocols.
Participants were fluid restricted starting 20–22 h on the day before the hypohydrated test sessions (HYT and HYH). The goal was for participants to start these sessions approximately 1%–2% hypohydrated as measured by BM changes. Participants were instructed to perform 60 min of the same type of exercise of their choice (elliptical, bike, or treadmill walking) during the afternoon before each test session. Twenty-four-hour dietary logs were collected to ensure that participants consumed the same meals before each test session. All test sessions were scheduled for the same time of day for each participant to remove any confounding factors due to time.
The four test sessions each began with the collection of the following measurements: BM, Usg, Ucol, Uosm, Tre, and HR (while standing quietly). The participants were equipped with a rectal thermometer, HR monitor (Polar Electro Inc., FT1, Kempele, Finland), and rucksack after these measurements were recorded. The participants then completed the first movement and postural control assessments (PRE) in the environmental chamber. After the first movement and the postural control assessments were complete, participants began the 90-min exercise protocol on the treadmill. During this time, HR, RPE, and Tre were measured every 15 min. This exercise protocol was intended not only to get the subjects’ Tre to a hyperthermic level but also to facilitate fatigue. During the euhydrated conditions (EUT and EUH), participants consumed fluids every 15 min in equal boluses during exercise according to their calculated sweat rate. Immediately at the cessation of walking, participants completed the second round of movement and postural control assessments (POST).
After POST, the participants put on a water-perfused suit. During the hot conditions (EUH and HYH), warm water was perfused continuously through the suits with the goal of maintaining an elevated Tre throughout the recovery period. During temperate conditions (EUT and HYT), cool water was perfused through the suits. While wearing the suit, participants rested in the chamber for 60 min and were restricted from fluid. The goal of this rest period was to allow the participants to physically recover from their exercise bout. The participants were able to remove their packs during this time and sit relaxed in a chair. As with during the exercise protocol, Tre and HR were measured every 15 min. Immediately after the 60-min recovery period, participants put the rucksack back on and completed the final movement and postural control assessments (REC). Participants then removed the pack, were weighed, removed their rectal probes, and submitted a final urine sample.
The movement assessment required participants to perform a standardized jump-landing task, which was videotaped. Video cameras were attached to the environmental chamber walls directly in front and to the side of the landing platform. While wearing the rucksack, participants jumped forward from a 30-cm-high box at a distance of 25% of their body height, landed in a target area, and immediately jumped for maximal vertical height. Each subject performed two practice jumps followed by three jump-landing trials. An additional jump was performed if participants did not land in the target area or the task was performed incorrectly. A single rater, blinded to condition and time, graded the videos at a later date using the Landing Error Scoring System (LESS) for potentially high-risk lower extremity movement patterns. The LESS is a valid and reliable clinical movement assessment tool to identify risk factors for ACL and other lower extremity injuries (23). The LESS has been validated in the military academy population (23) and correlates with subsequent injury risk in youth soccer players (21). A higher value for the LESS score indicates a greater number of landing errors performed and therefore indicates a “poor” jump-landing technique.
Postural Control Assessments
All three postural control assessments (PRE, POST, and REC) were identical and consisted of two postural control tests. The first postural control test used a modified version of the Balance Error Scoring System (BESS). The BESS has been shown to be a reliable measure of postural control that includes six positions (27). We modified the original protocol to remove the two double-limb positions because these positions result in the best performance. We also needed to make the assessment as fast as possible because the effects of fatigue on balance have been shown to be transient (7). Participants balanced for 20 s in four different positions, which differed based on stance and surface. Participants were instructed to keep their hands on their hips and their eyes closed for all four positions. The first position was a single leg stance on a firm surface (SLFirm), which required participants to keep their nondominant knee and hip flexed while they balanced on their dominant limb. The dominant limb was defined as the limb used to kick a ball for maximal distance. The tandem stance on a firm surface (TanFirm) was the second position tested, which involved participants standing with their nondominant heel in front of their dominant toes. The last two positions were a single leg stance and a tandem stance on a foam surface (SLFoam and TanFoam). The assessment was videotaped by a digital video camera placed directly in front of the participants.
A single rater, who was blinded to test condition, used the BESS to grade the videos at a later date. The number of errors each participant committed per position were tallied and summed per position and overall to result in a total BESS score. Errors were counted if the subject performed any of the following movements: lifted hands off the iliac crest, opened the eyes, stepped down, stumbled, moved the hip more than 30° of flexion or abduction during the single leg stances, lifted the forefoot or heel, or remained out of the testing position for more than 5 s.
The second postural control assessment was a unilateral dynamic landing test. Participants jumped forward off of their nondominant limb from a 30-cm-high box a distance of 25% of their body height and landed on their dominant foot in the center of a force plate with their hands on their hips. Immediately upon landing, participants were instructed to balance as quickly as possible and hold that position for 10 s. This test was performed until three trials were completed correctly. The trials were considered to be incorrect if the participant touched their nondominant foot to the ground, if their dominant foot slid forward on landing, or if the participant did not keep their hands on their hips. A nonconductive force plate (model 4060-NC; Bertec Corporation; Columbus, OH), controlled by Motion Monitor software (Innovative Sports Training, Inc., Chicago, IL), collected ground reaction force data during the dynamic task with a sampling frequency of 180 Hz.
Data Reduction and Analyses
The center of pressure (COP) x- and y-coordinates were computed using a Motion Monitor software (Innovative Sports Training, Inc., Chicago, IL). The force plate data were then exported into a customized software program (MatLab; The Mathworks, Boston, MA) and filtered using a low-pass, second-order 10-Hz Butterworth filter. COP average sway velocity (SV) was calculated as the average speed the COP moved within the base of support during the landing task. Elliptical sway area (ESA) was computed as the area defined by the minor and major axes of the ellipse that included 95% of the COP data points (7). The raters for the LESS and BESS data had clinical experience with the assessment tools and completed formalized training to ensure they were reliable. The errors for each BESS position were summed to result in a total BESS score as well as individual scores for each position. All data were analyzed using the Statistical Package for the Social Sciences (PASWStatistics 18.0; SPSS Inc., Chicago, IL) with an a priori alpha level of 0.05. We performed separate 4 × 3 (condition × time) repeated-measures ANOVA for each dependent variable. A Tukey HSD post hoc test was used to evaluate any significant differences.
The hypohydrated conditions (HYT and HYH) resulted in higher levels of dehydration compared with the hydrated conditions (EUT and EUH) as observed by BM loss and Uosm (Tables 1 and 2). The average Tre was similar at PRE and progressively increased throughout the exercise protocol during all conditions. The HYH condition resulted in the highest Tre at POST. Participants’ Tre at POST for the EUH and HYT conditions were similar and higher than the EUT condition. The water-perfused suit appeared to help maintain elevated Tre in the hot conditions because the REC Tre and PRE values for both the EUH and the HYH conditions were higher than the temperate conditions but lower than those of the POST values (Table 2). Fatigue, as operationally defined by higher RPE scores and HR, appeared to result from the 90-min exercise protocol for all conditions. Participants’ HR values at REC were similar to PRE values for all conditions, except the HYH condition (Table 1).
Landing error scoring system
We observed a significant interaction between time points and conditions for the total LESS score (F6,66 = 5.11, P < 0.001) (Fig. 1). LESS scores were highest during the HYH condition at POST compared with PRE and higher than both the HYT and the EUH conditions at POST and the EUT condition at REC. The LESS scores during the HYH condition at REC were higher versus the HYH condition at PRE, the HYT condition at POST, and the EUT condition at REC.
Balance error scoring system
Independent of condition, we observed differences between time points for the BESS score during the SLFirm (F2.22 = 5.37, P = 0.01) and TanFirm (F2,22 = 4.64, P = 0.02) positions as well as for the Total BESS score (F2,22 = 7.99, P = 0.002) (Fig. 2). The POST scores were significantly higher than the scores at PRE (Total and TanFirm) and REC (Total and SLFirm). Regardless of the time point, the HYH condition resulted in a higher total BESS score compared with the EUT and EUH conditions (F3,33 = 3.79, P = 0.02) and a higher BESS score during the TanFirm (F2,22 = 4.641, P = 0.02) and the TanFoam (F2,22 = 7.14, P = 0.001) positions compared with the EUT (TanFirm, TanFoam) and the EUH (TanFoam) conditions (Fig. 3). The EUH condition also had higher BESS scores during the TanFoam position compared with the EUT condition. Table 3 displays the results for all of the BESS measures across time and conditions.
ESA and SV
The HYH condition (ESA = 3.40 ± 1.21 cm2, SV = 6.62 ± 0.95 cm·s−1) consistently resulted in a larger ESA (F3,33 = 3.56, P = 0.048) and SV (F3,33 = 3.58, P = 0.02) compared with the HYT (ESA = 2.71 ± 0.66 cm2, SV = 6.06 ± 0.55 cm·s−1) and EUH (SV only; 6.16 ± 0.85 cm·s−1) conditions. Regardless of the condition, SV was slowest at PRE (5.89 ± 0.73 cm·s−1) compared with POST (6.53 ± 0.94 cm·s−1) and REC (6.35 ± 0.73 cm·s−1) (F2,22 = 7.61, P = 0.003).
Movement technique and postural control have been shown to be risk factors for lower extremity injury (12,17). The most important finding of this study was that movement technique during a landing task is negatively affected when an individual is hypohydrated and hyperthermic. These conditions also appear to impair balance ability, but to a lesser extent. However, exercising in a hot environment or while hypohydrated does not independently alter neuromuscular control, as measured by movement technique or balance ability. These findings emphasize the need for proper hydration during exercise in hot environments to reduce the risk of injury.
Influence of hypohydration in a hot environment
The LESS is a valid and reliable method of assessing lower extremity biomechanics (23), which have been associated with an increased risk of musculoskeletal injury (12,21). Instead of providing discrete measures of joint position, the LESS is a clinical tool that evaluates gross movement errors, such as medial knee displacement, hip or knee rotation, and limited sagittal plane motion. An increased overall LESS score indicates a higher number of movement errors and thus poor movement technique. After performing the exercise protocol in this study, participants demonstrated more movement errors when they were hypohydrated in a hot environment compared with when they were hypohydrated in a temperate environment or in a hot environment but euhydrated. This finding demonstrates the interacting effects of hypohydration and hyperthermia on diminishing movement technique. Injury prevention programs that have reduced lower extremity injury rates have also been shown to reduce LESS scores over time (6,22). In contrast, the changes in LESS scores observed in this study after hypohydrated participants exercised in a hot environment occurred on a single day using a within-subject design, which demonstrates the clinical significance of this finding.
During the HYH condition and regardless of time, participants consistently demonstrated postural control deficits, as measured by an increase in total and tandem stance BESS scores and both dynamic landing task measures. Although no significant interactions between conditions and time points were observed for any of these balance measures, we believe the POST and the REC time points were responsible for the observed main effect for condition when both hyperthermia and hypohydration were present. The balance measures appear to be more variable and not as sensitive as the LESS score in evaluating neuromuscular control deficits from hypohydration and hyperthermia, which limit the ability to detect a significant interaction with the current sample size. To our knowledge, this is the first study to evaluate the effects of hyperthermia and hypohydration on balance without the confounding influence of fatigue.
Influence of fatigue
Several studies have observed impaired movement and postural control after intense exercise protocols and concluded fatigue increases injury risk (2,7,18,20). In light of the current findings, it is possible that the results of some of these studies may have been confounded by the presence of hypohydration and hyperthermia. To our knowledge, this is the first study to evaluate rectal temperature and hydration status during exercise while studying movement technique and postural control. The observed impairments in movement technique remained after 60 min of rest during the hypohydrated, hot environment condition, suggesting that the movement technique deficits were not due to fatigue but instead due to the combined effects of hypohydration and hyperthermia. Previous studies may have used more intense exercise protocols than the current protocol, which may explain why we did not find movement technique deficits due to fatigue alone. Therefore, future research should further evaluate the role of fatigue, independent of hyperthermia or hypohydration.
Although fatigue apparently did not independently impair movement technique, our results demonstrate that fatigue, regardless of hydration status or environmental conditions, impairs balance ability. This finding is consistent with previous studies and appears to be a transient effect. We are not aware of any previous study examining the effects of fatigue on postural control that subsequently controlled for the effects of hypohydration or an elevated rectal temperature, or even measured hydration or body temperature. In the current study, all conditions regardless of hydration status or environmental conditions caused postural control impairments immediately after the 90-min exercise protocol. The total BESS scores were greater at POST compared with PRE and REC. Although SV was higher at POST compared with PRE, there was no difference between SV at POST and REC. This suggests that SV impairments do not seem to completely recover after the exercise task.
Hypohydration may impair neuromuscular control by affecting the cognitive ability and the vestibular system, which is one of three main systems responsible for balance (14). The current findings suggest that hypohydration alone does not impair neuromuscular control through movement technique or balance ability. To our knowledge, this is the first study to evaluate the effects of hypohydration on movement technique, and previous literature examining the influence of hypohydration on balance ability is inconclusive (3,14,25). Previous literature has not controlled for body temperature and few have controlled fatigue, which may explain why the results are inconclusive. Both hypohydrated conditions in the current study (HYH and HYT) did not result in decreased balance at PRE, when fatigue and hyperthermia were absent. Further, participants only demonstrated diminished balance during the HYT condition at POST, which was consistent across conditions, indicating this impairment was due to fatigue and not hypohydration. Our findings suggest that hypohydration did not impair postural control.
We believe this is the first study to isolate the effects of hyperthermia on balance ability and movement technique. Although we did not observe a significant interaction between time points and conditions for the postural control measures, we did observe diminished postural control (increased BESS scores during TanFoam) when participants were euhydrated and exercised in a hot environment (EUH condition) compared with when they were euhydrated and exercised in a temperate environment (EUT condition). We believe that the elevated BESS scores at POST and REC are driving this significant condition main effect, but intersubject variability prevented us from observing a significant interaction. During the EUH condition, participants’ rectal temperatures at REC were elevated compared with the EUT and HYT conditions. We believe this elevation was due to hyperthermia alone because participants were euhydrated and the REC measurement was taken 60 min after the cessation of exercise. This finding may be clinically important as it suggests that exercising in a hot environment can impair one aspect of balance.
Limitations and future research
A limitation of this study is that the subject sample consisted of aerobically trained adult men. Future research should evaluate if similar effects are demonstrated in women and less-trained individuals. Participants’ neuromuscular control was assessed while wearing a heavy rucksack. This was performed to simulate the external loads of individuals in the military and some that athletes frequently encounter. Although the load itself could impair postural control, we do not believe it greatly limits the generalizability of this study’s findings as the rucksack was present at all time points and during all conditions. RPE scores and HR have been used in multiple studies to confirm fatigue after an exercise protocol (2,7). We observed similar HR values during the assessments before the exercise protocol and after the recovery period but elevated RPE and HR values immediately after the exercise protocol. These findings confirm that the exercise protocol in the study caused the participants to be fatigued temporarily during the POST test, as defined by elevated HR and RPE values.
Teaching proper movement techniques during sport-specific tasks, such as the jump-landing task, and training balance are emphasized during lower extremity injury prevention programs. These programs have been shown to reduce lower extremity and ACL injury risk (9,16,19) as well as decrease LESS scores (6) and improve balance ability (4,5). Therefore, the findings from this study may have significant implications for injury prevention efforts. Hypohydration occurs frequently during sport participation and military endeavors. Further research should evaluate if lower extremity injury prevention programs can attenuate the possible increased risk of injury present when an individual is hypohydrated and exercising in the heat. We also recommend that individuals focus on hydrating properly during exercise in the heat not only to enhance performance and protect themselves from heat-related illness but also to attenuate lower extremity injury risk.
The authors acknowledge the university’s faculty grant program for funding this study.
None of the authors declare any conflicts of interest.
The results of the present study do not constitute endorsement by the American College of Sports Medicine.
1. Armstrong LE, Maresh CM, Gabaree CV, et al. Thermal and circulatory responses during exercise: effects of hypohydration, dehydration, and water intake. J Appl Physiol. 1997; 82 (6): 2028–35.
2. Chappell JD, Herman DC, Knight BS, Kirkendall DT, Garrett WE, Yu B. Effect of fatigue on knee kinetics and kinematics in stop-jump tasks. Am J Sports Med. 2005; 33 (7): 1022–9.
3. Derave W, De Clercq D, Bouckaert J, Pannier JL. The influence of exercise and dehydration on postural stability. Ergonomics. 1998; 41 (6): 782–9.
4. DiStefano LJ, Clark MA, Padua DA. Evidence supporting balance training in healthy individuals: a systemic review. J Strength Cond Res. 2009; 23 (9): 2718–31.
5. DiStefano LJ, Padua DA, Blackburn JT, Garrett WE, Guskiewicz KM, Marshall SW. Integrated injury prevention program improves balance and vertical jump height in children. J Strength Cond Res. 2010; 24 (2): 332–42.
6. DiStefano LJ, Padua DA, DiStefano MJ, Marshall SW. Influence of age, sex, technique, and exercise program on movement patterns after an anterior cruciate ligament injury prevention program in youth soccer players. Am J Sports Med. 2009; 37 (3): 495–505.
7. Fox ZG, Mihalik JP, Blackburn JT, Battaglini CL, Guskiewicz KM. Return of postural control to baseline after anaerobic and aerobic exercise protocols. J Athl Train. 2008; 43 (5): 456–63.
8. Gauchard GC, Gangloff P, Vouriot A, Mallie JP, Perrin PP. Effects of exercise-induced fatigue with and without hydration on static postural control in adult human subjects. Int J Neurosci. 2002; 112 (10): 1191–206.
9. Gilchrist J, Mandelbaum BR, Melancon H, et al. A randomized controlled trial to prevent noncontact anterior cruciate ligament injury in female collegiate soccer players. Am J Sports Med. 2008; 36 (8): 1476–83.
10. Gonzalez-Alonso J. Hyperthermia impairs brain, heart and muscle function in exercising humans. Sports Med. 2007; 37 (4–5): 371–3.
11. Hawkins RD, Hulse MA, Wilkinson C, Hodson A, Gibson M. The association football medical research programme: an audit of injuries in professional football. Br J Sports Med. 2001; 35 (1): 43–7.
12. Hewett TE, Myer GD, Ford KR, et al. Biomechanical measures of neuromuscular control and valgus loading of the knee predict anterior cruciate ligament injury risk in female athletes: a prospective study. Am J Sports Med. 2005; 33 (4): 492–501.
13. Hootman JM, Macera CA, Ainsworth BE, Addy CL, Martin M, Blair SN. Epidemiology of musculoskeletal injuries among sedentary and physically active adults. Med Sci Sports Exerc. 2002; 34 (5): 838–44.
14. Lion A, Bosser G, Gauchard GC, Djaballah K, Mallie JP, Perrin PP. Exercise and dehydration: A possible role of inner ear in balance control disorder. J Electromyogr Kinesiol. 2010; 20 (6): 1196–202.
15. Lohmander LS, Ostenberg A, Englund M, Roos H. High prevalence of knee osteoarthritis, pain, and functional limitations in female soccer players twelve years after anterior cruciate ligament injury. Arthritis Rheum. 2004; 50 (10): 3145–52.
16. Mandelbaum BR, Silvers HJ, Watanabe DS, et al. Effectiveness of a neuromuscular and proprioceptive training program in preventing anterior cruciate ligament injuries in female athletes: 2-year follow-up. Am J Sports Med. 2005; 33 (7): 1003–10.
17. McGuine TA, Greene JJ, Best T, Leverson G. Balance as a predictor of ankle injuries in high school basketball players. Clin J Sport Med. 2000; 10 (4): 239–44.
18. McLean SG, Fellin RE, Suedekum N, Calabrese G, Passerallo A, Joy S. Impact of fatigue on gender-based high-risk landing strategies. Med Sci Sports Exerc. 2007; 39 (3): 502–14.
19. Myklebust G, Engebretsen L, Braekken IH, Skjolberg A, Olsen OE, Bahr R. Prevention of anterior cruciate ligament injuries in female team handball players: a prospective intervention study over three seasons. Clin J Sport Med. 2003; 13 (2): 71–8.
20. Nardone A, Tarantola J, Giordano A, Schieppati M. Fatigue effects on body balance. Electroencephalogr Clin Neurophysiol. 1997; 105 (4): 309–20.
21. Padua D, Marshall S, Beutler A, et al. The Landing Error Scoring System (LESS) prospectively identifies ACL injury. J Athl Train. 2010; 45 (5): S39.
22. Padua DA, DiStefano LJ, Marshall SW, Beutler AI, de la Motte SJ, DiStefano MJ. Retention of movement pattern changes after a lower extremity injury prevention program is affected by program duration. Am J Sports Med. 2012; 40 (2): 300–6.
23. Padua DA, Marshall SW, Boling MC, Thigpen CA, Garrett WE Jr, Beutler AI. The Landing Error Scoring System (LESS) is a valid and reliable clinical assessment tool of jump-landing biomechanics: the JUMP-ACL Study. Am J Sports Med. 2009; 37 (10): 1996–2002.
24. Pal S, Besier TF, Draper CE, et al. Patellar tilt correlates with vastus lateralis: vastus medialis activation ratio in maltracking patellofemoral pain patients. J Orthop Res. 2012; 30 (6): 927–33.
25. Patel AV, Mihalik JP, Notebaert AJ, Guskiewicz KM, Prentice WE. Neuropsychological performance, postural stability, and symptoms after dehydration. J Athl Train. 2007; 42 (1): 66–75.
26. Price RJ, Hawkins RD, Hulse MA, Hodson A. The Football Association medical research programme: an audit of injuries in academy youth football. Br J Sports Med. 2004; 38 (4): 466–71.
27. Riemann BL, Guskiewicz KM. Effects of mild head injury on postural stability as measured through clinical balance testing. J Athl Train. 2000; 35 (1): 19–25.