The knee is commonly injured with multiple sports, and joint immobilization often must be implemented in the initial management to protect damaged tissues and alleviate pain (1,2). The acute unstable knee, anterior cruciate ligament tear, patellar dislocation, and other acute traumatic knee injuries initially require complete immobilization (1,2). After medical and/or surgical management of the acute injury, the athletes face a long postoperative rehabilitation time that includes joint remobilization (3). However, prolonged use of a cast or a knee orthosis restricting motion after knee injury or surgery risks many complications (4). Prolonged immobilization has detrimental effects on cartilage, bone, and soft tissues and can result in a loss of range of motion (ROM) (5). Flexion contractures are common complications after knee replacement and anterior cruciate ligament reconstruction (6,7). The loss of knee extension increases joint contact pressures, quadriceps muscle activity, fatigue, and impairs gait, limiting performance for active athletes (5,8–12). Quantitative data on anatomical structures limiting knee mobility are limited but necessary to design and test new interventions to restore knee joint mobility postinjury. The limited number of clinical studies has precluded the use of human samples (13). In turn, the rat model exhibits similar anatomy and physiology to the human knee and has shown ROM limitations in response to immobilization (13,14).
Experimental models of knee joint contractures showed that long durations of immobilization caused contractures (14). The tissues responsible for the limitation in ROM have been grouped into myogenic and arthrogenic categories (11,15,16). Myogenic restrictions are caused by muscle, tendon and fascia, whereas, arthrogenic restrictions are caused by bone, cartilage, synovium, capsule, and ligaments (15,16). After division of the skin and muscles, the remaining restriction in knee extension can be attributed to arthrogenic restrictions (15,17). Previous experimental studies have documented decreased ROM with increasing durations of immobility (14,16), and as well as decreased posterior synovial length beyond 2 to 4 wk of immobilization (8,18). The importance of the posterior capsule in limiting knee extension during joint contractures has been documented in a rat model (8,16,17); with posterior capsulotomy restoring some knee extension deficits (19–21). The anatomical changes of the posterior capsule with immobilization support investigating its reversibility during remobilization after injury (22,23).
A previous exhaustive temporal study quantified the ROM of knees during unassisted recovery, after immobilization (17). The results indicated that knees immobilized for 1 and 2 wk recovered full range of extension; however, knees immobilized for more than 2 wk, had no significant recovery with remobilization.
The present study investigated anatomical changes in the posterior capsule of rat knee joints with contractures during remobilization and correlated those with previously published ROM data from the same specimen (17). Our objectives were to 1) measure the posterior knee capsule length after 1 to 32 wk of immobilization and 1 to 48 wk of remobilization and 2) correlate the posterior capsule length measurements with previously published ROM data. Our hypotheses were that 1) the posterior capsule shortening after long durations of immobilization will not reverse after any duration of unassisted remobilization, and 2) shorter posterior capsules correlate positively with reduced knee ROM in the remobilization phase after immobilization.
MATERIALS AND METHODS
The experimental method was previously detailed by Trudel et al. (17) and approved by the Animal Care Committee (ME-2461). In summary, 259 male Sprague–Dawley rats (350 g) had one knee extra-articularly fixed with a Delrin® plate spanning from proximal femur to distal tibia at a 45° angle for one of six durations: 1, 2, 4, 8, 16, or 32 wk (Fig. 1). The side of surgery was alternated. The contralateral knees served as the control group. Immobilization was lifted by removing the plate and each period of immobilization was followed by four different durations of spontaneous remobilization. Rats were allowed free activity in their cages for zero, one, two, or four times the duration of immobilization, with exception to the longest durations of immobilization (Fig. 1). At the end of the remobilization period, the rats were killed by carbon dioxide inhalation and the knees were mechanically tested for angle of knee extension using a fully automated arthrometer with a force of 12.5 N·cm (24) and immediately harvested. The ROM measurements of the knee in extension after division of skin and muscles were used in this study to attribute the remaining knee extension deficit to arthrogenic restrictions. Groups are defined as week–week, where the first number is the duration of immobilization and the second is the duration of remobilization (e.g., group 2–4 was immobilized for 2 wk and remobilized for 4 wk). We measured the posterior capsule length in the same rat knees that had ROM measured (17). It was previously reported that 250 rats had been used for ROM the study; however, due to the lengthy experimental design, additional rats were included to account for potential loss and replacement. As a result, nine additional rats were available for histological analysis and used in the current study, despite not being tested for ROM.
Tissue preparation and staining
The knee joints and surrounding tissues were removed en bloc, fixed in Bouin’s solution (in its natural repositioning after remobilization) for 24 h, decalcified in 10% Tris-ethylenediaminetetraacetic acid solution for 2 months, and embedded in low melting point paraffin (18). Standardized serial sections at the medial mid-condylar level were made in the sagittal plane. The 7-μm sections were stained with 1% Alcian Blue for 5 min and 0.5% Direct Red for 5 min. Alcian blue was selected for staining to create an optimal differentiation between the intimal and subintimal layers of the capsule; Direct Red acted as a counterstain (8).
Histomorphometric analyses: measurement of posterior capsule length
The mounted sections were examined at a low magnification (3.3–6.6×) on a light microscope (Olympus BH-2, Tokyo) and histologically analyzed using imaging software ImageJ (NIH, Bethesda, MD). This study focuses on the posterior capsule because we are studying knee flexion contractures. The synovial intima length of the posterior capsule was measured. The femoral and tibial sections of the posterior synovial length were measured separately, with the medial meniscus as the anatomical landmark used for the division. The posterior femoral synovial length was measured from the posterior-superior horn of the medial meniscus to the synoviocartilage junction on the posterior femur and the posterior tibial synovial length was measured from the posterior-inferior horn of the meniscus to the posterior tibia synoviocartilage junction [see Figure, Supplemental Digital Content 1, Anatomical structures and orientation of the rat knee joint, illustrating the histological measurement, http://links.lww.com/MSS/B380]. Anatomically, the tibial posterior capsule is shorter than the femoral section (see Figures, Supplemental Digital Content 1 and 2, Femoral and tibial posterior capsule length [mm] of rat knee joints after a fixed duration of immobilization and increasing durations of remobilization, illustrating this difference, http://links.lww.com/MSS/B380 and http://links.lww.com/MSS/B381). Results from both sections are combined to equal the posterior capsule length. Capsule length was measured by the same person blinded to the experimental group and slides were randomized before analysis.
All capsule length data were expressed as mean ± standard deviation. Statistical analysis was conducted using SPSS version 24.0 (IBM Corp., Armonk, NY). Differences between experimental and contralateral knees were compared at each time point by paired t-test. The temporal effects of recovery among groups were compared using a one-way ANOVA followed by Tukey’s post hoc test. In the ANOVA, the dependent variable was posterior capsule length and the independent variable was time of immobilization/remobilization. Values of P < 0.05 were considered statistically significant.
Pearson correlation coefficient analysis was conducted to determine the strength of the linear relationship between posterior capsule length and ROM data previously published from the same samples (17) after immobilization and remobilization. All immobilization groups were pooled together for a fixed duration of remobilization (0, 8, or 16 wk) and posterior capsule length was paired with individual ROM measurements for each rat knee. The total, femoral, and tibial posterior capsule lengths were correlated separately with ROM. Rats that did not have both ROM and capsule length measurements were excluded from analysis. Multiple correlations were accounted for using a single step post hoc Bonferroni correction. Values of (P < 0.003) were considered statistically significant.
Of 518 knees, 74 (32 experimental and 42 contralateral knees; seven rats had both knees excluded = 14 knees or seven rats) were damaged by prior mechanical testing or histological processing, leaving 444 knee specimens from 252 rats for histomorphological analysis. The distributions per group are illustrated in Table, Supplemental Digital Content 3, Summary of statistics comparing posterior capsule length of different groups of experimental and contralateral knees with a fixed duration of immobilization and increasing durations of remobilization, which shows sample sizes at http://links.lww.com/MSS/B382.
The contralateral groups, after immobilization and remobilization, showed a folded posterior joint capsule on both the femoral and tibial sites (Fig. 2); synovial folds were in close proximity. Immobilized groups showed that synovial folds had adhered together, leading to decreased posterior capsule length.
Posterior capsule length after fixed durations of immobilization with increasing durations of remobilization
Quantitative measures of the posterior capsule length after various durations of knee immobilization and remobilization are illustrated in Figure 3. Posterior capsule length of knees immobilized for 1 wk followed by 1 to 4 wk of remobilization were comparable to contralateral knees (all P > 0.05; Fig. 3A). In knees immobilized for 2 wk and remobilized for 2 and 8 wk, the posterior capsules were shorter than the corresponding contralateral knees (P < 0.05; Fig. 3B). Knees immobilized for 2 wk also had a longer posterior capsule after 4 wk of remobilization when compared with no remobilization (group 2–0) (P < 0.05; Fig. 3B).
The shorter posterior capsule of knees immobilized for 4 wk failed to recover its length after any duration of remobilization (4, 8, and 16 wk), when compared with no remobilization (4–0) (all three P > 0.05; Fig. 3C). The posterior capsules of knees immobilized for 4 wk and remobilized for 0, 8 and 16 wk were also significantly shorter than that of contralateral knees (all 3 P < 0.05; Fig. 3C). For knees that were immobilized for 8, 16, or 32 wk, the posterior capsule failed to significantly increase in length after any duration of remobilization up to 48 wk, when compared with no remobilization (eight comparisons P > 0.05; Fig. 3D–F), with the exception of group 16 to 32 (P < 0.05). The posterior capsule of knees immobilized for 8, 16, or 32 wk and remobilized for any duration up to 48 wk were also significantly shorter than corresponding contralateral knees (all 12 comparisons P < 0.05; Fig. 3D–F). Immobilization for 1, 2, 4, 8, 16, and 32 wk and remobilization up to 48 wk did not affect the posterior capsule length of contralateral knees when compared with no remobilization (all P > 0.05).
Posterior capsule length after increasing durations of immobilization with fixed duration of remobilization
Despite 8 or 16 wk of remobilization, the posterior capsule length of knees immobilized for 2, 4, 8, 16, or 32 wk remained shorter than the contralateral knee (all 8 comparisons P < 0.05). Also, the posterior capsule of immobilized knees shortened as the duration of immobilization was increased. For knees remobilized for 8 wk, the posterior capsule length was significantly shorter after 16 wk of immobilization when compared with the earliest duration of immobilization (2–8) (P < 0.05 Fig. 4A). Knees remobilized for 16 wk had significantly shorter posterior capsule lengths after 8, 16, and 32 wk of immobilization, when compared with the earliest duration of immobilization (4–16) (all three P < 0.05; Fig. 4B). Posterior capsule length of knees contralateral to the knees immobilized for 2, 4, 8, 16, and 32 wk and remobilized for 8 or 16 wk were unchanged (all P > 0.05).
Femoral and tibial posterior capsule length
Changes in posterior capsule length were mainly attributable to changes to the longer posterosuperior (femoral) section of the posterior capsule and less to the posteroinferior (tibial) section [see Figures, Supplemental Digital Content 2 and 4, Femoral and tibial posterior capsule length (mm) of rat knee joints after increasing durations of immobilization with a fixed duration of remobilization, which shows differences in length at http://links.lww.com/MSS/B381 and http://links.lww.com/MSS/B383].
Correlation between posterior capsule length and ROM
Posterior capsule length positively correlated with range of knee extension in all immobilization groups combined (r = 0.542; P < 0.001) (Table 1, Fig. 5). In knees immobilized for 2, 4, 8, and 16 wk followed by 8 wk of remobilization, the reduced posterior knee capsule length positively correlated with the range of knee extension but failed to reach statistical significance after correcting for multiple comparisons (r = 0.456; P = 0.007). For knees immobilized 4, 8, 16, and 32 wk and remobilized for 16 wk, the reduced posterior knee capsule length correlated with decreased knee extension (r = 0.541; P < 0.001). In the contralateral knees of the 16-wk remobilization group, no significant correlation was measured between posterior knee capsule length and the range of knee extension (r = 0.342; P = 0.031).
We report reversibility of posterior capsule length shortening after knee contractures induced by immobilization of 2 wk or less. However, unassisted remobilization of any duration, even when four times longer than the period of immobilization, failed to reverse the posterior capsule shortening caused by immobilization longer than 2 wk, confirming our first hypothesis. This finding shows a biological difference between short and long durations of immobilization in response to remobilization. Second, posterior capsule shortening correlated with loss of knee range of extension, both in knees that were and those that were not remobilized, confirming our second hypothesis. The current comprehensive study adds to the literature multiple durations of immobilization, up to 32 wk, and of remobilization up to 48 wk. The range of immobilization and remobilization durations is compatible with the clinical presentation of patients treated for weeks and months after their knee injury.
Posterior capsule length shortening
Our data add quantitative data to the literature supporting that the posterior knee capsule changes are irreversible, at least for unassisted recovery. Two experimental studies have reported irreversibility of capsule shortening after knee immobilization and remobilization. Kaneguchi et al. (25) used transarticular Kirschner wires to immobilize rat knees for 3 wk and remobilized up to 2 wk. They found that the posterior capsule length decreased after immobilization and further decreased after remobilization. Furthermore, they showed that the arthrogenic contracture had continued to develop during the short period of remobilization. Ando et al. (26) adopted our method for internal fixation, processing, and histological assessment to show similar results using 16 wk as the single duration of remobilization with 1 to 16 wk of immobilization (26). These and other experiments, as well as clinical reports, have established the posterior capsule as a major contributor to the lack of knee extension in immobility-induced knee contractures (18–21,27).
Our study establishes the synovial layer as a valid and responsive surrogate marker of underlying posterior capsule contribution to an arthrogenic limitation in joint contractures secondary to immobility. Previous studies have explained the shortening of the posterior capsule as a result of adhesions of synovial villi to neighboring synovial villi, or to articular cartilage after immobilization (14,18). Because the knee is immobilized in flexion, the posterior part of the joint is not under tension, allowing for the loose synovial layer to fold and adhere to one another (14,18). Moreover, the lack of tension permits capsular cellular elements such as fibroblasts, synoviocytes, and adipocytes to proliferate, which impacts changes in proteoglycans, collagen proteins, and crosslinks between collagen fibers in the extracellular matrix (14,16,23). Additionally, the rabbit model of posttraumatic joint contracture has shown increased number of myofibroblasts in the posterior capsule after immobilization (28,29). These changes all contribute to the fibrosis and stiffness of the posterior capsule, which further increases the resistance to joint motion (14,18,23,28). The importance of capsular adhesions can be appreciated because the shortened capsule length persisted after remobilization following immobilization beyond 2 wk. In this study, shortening of posterior capsule length occurred predominately in the femoral part of the capsule (see Supplemental Figures 2 and 3, Supplemental Digital Content 2 and 4, showing this change, http://links.lww.com/MSS/B381 and http://links.lww.com/MSS/B383). The femoral posterior capsule is anatomically longer than the tibial capsule, permitting more synovial folds to coalesce, more synovial-synovial contact, and opportunities for adhesions to form between folds.
Posterior capsule length and knee ROM in extension
Range of motion is the main functional outcome measure when evaluating the severity of joint contractures (22), and the only one available to clinicians treating athletes with after knee injury. Pairing the anatomical posterior capsule length data with the range of knee motion allowed correlating the mechanical limitation to an articular structure. Correlating posterior capsule length with ROM data in the same knee joints greatly reduces data variability. Previously published data showed decreased ROM in knees immobilized for 1 to 2 wk (17). However, remobilization led to recovery in the range of knee extension, reaching levels comparable to the contralateral. The ROM tested before myotomy allowed distinguishing the restrictions mainly of myogenic origin, which led to reduced ROM after short durations of immobilization, with little contribution from arthrogenic structures (14–17). The current study confirms that intraarticular synovial length changes after short periods of immobilization were reversible and support that myogenic changes might account for the temporary decrease in knee range of extension (17). However, as arthrogenic contractures develop, the loss of knee ROM becomes irreversible (17). In this study, posterior capsule length positively correlated with knee range of extension after myotomy as durations of immobilization increased, regardless of whether the knees were remobilized or not. This reinforces the contribution of the posterior capsule to arthrogenic contractures. The posterior capsule length of contralateral knees also showed a weaker correlation with knee extension. Possible reasons include aging, causing both reduced ROM and synovial length, or gait adaptation, by flexing the knee opposite to the immobilized knee to compensate for discrepancy in leg length (12). The stronger correlation in immobilized legs confirms that the correlations we report are not due to age only. In our study, we applied a Bonferroni correction, a very conservative method, to account for the multiple correlation analyses performed. Positive correlations between posterior capsule length and ROM were measured in all remobilization groups but failed to reach significance in the 8-wk remobilization group. The positive correlation between the capsule structure and ROM after immobilization and remobilization highlights the functional importance of the reduction in length of the posterofemoral capsule.
Knee injuries are most common in sports medicine and many are treated with immobilization during conservative management or after surgery. The development of a knee joint contracture poses a significant challenge to athletes and the treating team, which may constitute a career-ending complication for runners, jumpers, and cyclists (5). Current rehabilitation treatments for established knee joint contractures include sustained stretching and exercises to increase ROM, whereas severe contractures may require surgical intervention (11,22). We provided quantitative data pointing to an anatomical deficit, the posterior knee capsule shortening, which correlated with the lack of knee extension after immobilization. Progressive capsule shortening with incremental durations of immobilization was an irreversible process that correlated with irreversible arthrogenic contractures. Unassisted remobilization was insufficient to restore posterior capsule length and range of knee extension when immobilized beyond 2 wk. The data indicated a short window of opportunity for intervention where anatomical reversibility of the capsule adhesions was possible. This study provides experimental evidence for minimizing the duration of knee immobilization after a knee injury. The data also support that should immobilization extend past 2 wk, as it is the case for many acute traumatic knee injuries (30), unassisted remobilization may be insufficient to reverse the anatomical and ROM changes. Assisting the passive and active knee mobilization of the athlete is recommended. Considering the use of an animal model, this study is limited by the use of a quadruped rat model, whose knee’s habitual position is in flexion, which may cause the knee to be more resistant to flexion contractures (17). However, the similar rat knee anatomy and function in comparison to human provides valuable knowledge about the lack of reversibility after the development of a flexion contracture caused by prolonged immobilization.
Immobilized knees developed flexion contractures characterized anatomically by shortening of the posterior capsule that correlated with the mechanical lack of knee extension. This exhaustive study provided quantitative and temporal evidence that both joint alterations were irreversible by unassisted remobilization when the duration of knee immobilization exceeded 2 wk. Interventions aimed at restoring knee extension must be implemented as unassisted remobilization will not reverse knee flexion contractures.
Support for this work was provided by Canadian Institutes of Health Research Grant MOP 97831 to G. T. and O. L. Author H. Z. is supported by the Hans K. Uhthoff MD, FRCSC, Graduate Fellowship. The authors thank W. Yie for preparation of the rat knee sections.
No conflicts of interest, financial or otherwise, are declared by the author(s). The authors declare that the results of the present study are presented clearly, honestly, without fabrication, falsification or inappropriate data manipulation, and does not constitute an endorsement by ACSM.
G. T., O. L., and H. K. U. participated in the conception and design of research. H. Z. performed the experiments. H. Z. analyzed the data. H. Z., G. T., and O. L. interpreted results of experiments. H. Z. prepared the figures and drafted the article. H. Z., G. T., H. K. U., and O. L. edited and revised the article. H. Z., G. T., H. K. U., and O. L. approved final version of the article.
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POSTERIOR JOINT CAPSULE; KNEE; RANGE OF MOTION; FLEXION CONTRACTURE; REHABILITATION
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