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| REVIEW ARTICLE |
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| Year : 2020 | Volume
: 10
| Issue : 1 | Page : 10-18 |
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Concussion and lower extremity injury risk following return to activity: A systematic review
Jessica Buttinger1, Jason Mihalik2, Leila Ledbetter3, Mallory Faherty4, Timothy Sell4
1 Duke University, Department of Orthopaedic Surgery, Michael W. Krzyzewski Human Performance Laboratory; Central Michigan University College of Medicine
2 Duke University School of Medicine, Medical Library
3 The University of North Carolina, Department of Exercise and Sport Science, Matthew A. Gfeller Sport-Related Traumatic Brain Injury Research Center
4 Duke University, Department of Orthopaedic Surgery, Michael W. Krzyzewski Human Performance Laboratory
| Date of Submission | 21-May-2020 |
| Date of Acceptance | 18-Sep-2020 |
| Date of Web Publication | 21-May-2021 |
Correspondence Address:
Ms. Jessica Buttinger
Central Michigan University College of Medicine, 1280 East Campus Dr, Mt Pleasant, MI 48858, USA
 Source of Support: None, Conflict of Interest: None
DOI: 10.4103/DORJ.DORJ_16_20
Aim: The purpose of this systematic review is to present the evidence examining concussion and subsequent lower extremity injury (LEI) risk, and to provide a clinically relevant interpretation of the existing literature for sports medicine clinicians. We hypothesize that there is sufficient high-quality evidence providing an association between concussion and subsequent LEI risk.
Background: In active individuals who have suffered a concussion, even after acute symptoms resolve, the long-term consequences and cognitive deficits that persist remain a pervasive topic of study in sports medicine research. As more studies indicate a risk of secondary injury following a concussion, specifically a risk of LEI, a review of the literature is necessary to bring the latest research into discussion.
Review Results: Of the 459 studies reviewed for eligibility, 10 articles were accepted for systematic review and graded for quality. Overall, eight of the ten studies meeting the inclusion criteria demonstrated an association between concussion and LEI. The risk of LEI following a concussion ranged in studies with odds ratios ranging from 1.72 to 2.48, hazards ratios ranging from 1.47 to 4.07, and the incident rate ratio ranging from 1.97 to 2.02 in athletes who had acquired a concussion versus those who did not.
Conclusion: Taken together, there is enough evidence of sufficient quality to determine that there is an association between concussion and the subsequent risk of acquiring a lower-extremity injury. This systematic review suggests care should be taken in future studies to assess the contributing factors that may predispose an individual to lower extremity injuries following a concussion.
Clinical Significance: Concussions and the subsequent risk of LEI remain a growing concern for sports medicine providers. Our study suggests that there is a need to further investigate the mechanistic processes that may be predisposing an individual to subsequent lower extremity injuries following a concussion, and if this risk can be reduced with appropriate postconcussion care.
Keywords: Athletics, concussion, return to play
How to cite this article:
Buttinger J, Mihalik J, Ledbetter L, Faherty M, Sell T. Concussion and lower extremity injury risk following return to activity: A systematic review. Duke Orthop J 2020;10:10-8 |
How to cite this URL:
Buttinger J, Mihalik J, Ledbetter L, Faherty M, Sell T. Concussion and lower extremity injury risk following return to activity: A systematic review. Duke Orthop J [serial online] 2020 [cited 2023 Jun 2];10:10-8. Available from: https://www.dukeorthojournal.com/text.asp?2020/10/1/10/316557 |
| Introduction | |  |
Sport-related concussions are a significant health concern for active individuals. An estimated 1.6–3.8 million recreation- and sport-related concussions are sustained annually in the USA,[1] and the incidence seems to be increasing over the past two decades.[2],[3] Postconcussion problems are significant, posing consequences that effect an individual's athletic participation,[4] neurocognitive performance and processing speed,[5],[6] psychological issues (mood and personality),[7],[8] as well as increasing the risk for a secondary concussion.[9]
Numerous studies describe persistent deficits in motor control and neuromuscular function following a concussion,[10],[11],[12],[13],[14] including changes in postural stability,[15],[16],[17],[18],[19] motor control strategies such as dual-task performance and gait analysis,[20],[21],[22],[23],[24],[25],[26] as well as muscular strength.[27],[28] Riemann et al.[16] reported that concussed participants showed significantly higher postural instability than matched nonconcussed controls. In addition, Howell et al.[22] identified concussed athletes demonstrating altered gait during dual task walking following a complete return to activity based on traditional clinical measures of concussion. Taken together, motor control and neuromuscular function deficits may compromise functional joint stability. Since evaluating these outcomes following concussion is not yet pervasive in clinical sports medicine, it is possible individuals suffering from sports-related concussion are prematurely returning to activity and thus, may be at risk for secondary injuries.
Functional joint stability is essential to safe and injury free participation in sports, recreational activities, and exercise. This is well established in the hip, knee, and ankle literature as many activities place significant biomechanical demands on the lower extremity.[29],[30],[31] Functional joint stability can be defined as the state of a joint remaining in or promptly returning to proper alignment by equalizing forces.[32] It is a complex process requiring synergy between bones, joint capsules, ligaments, muscles, tendons, and sensory receptors,[33] as well as neuromuscular control of the skeletal muscles crossing the joint.[32] This neuromuscular control requires the musculoskeletal and nervous systems to dynamically interact.[34] Injury or persistent deficits at anywhere in this system (central nervous system or the peripheral joint) may compromise an individual's ability to maintain functional joint stability and lead to injury. Sports-related concussion may introduce dysfunction in these complex systems, leading to the recent reports linking concussion to subsequent musculoskeletal injury.[4],[10],[11],[12],[13],[14],[35],[36],[37],[38]
Scientific literature has established that concussions lead to deficits in neuromuscular function and motor control. A timeline for a full recovery in these functions has not yet been identified, but mounting evidence suggests deficits persist even beyond traditional definitions of clinical recovery and full return to activity. A subsequent compromise in functional joint stability may have short- and long-term musculoskeletal health implications, ranging from increasing lower extremity injury (LEI) risk (acutely) and osteoarthritis (chronically) secondary to those injuries. The purpose of this systematic review is to determine an association between concussion and subsequent LEI risk, and to provide a clinically relevant interpretation of the existing literature for sports medicine clinicians. We hypothesize there is sufficient high-quality evidence providing a strong association between concussion and subsequent LEI risk. If our hypothesis is correct, we would suggest future studies should focus on this aspect of concussion risk, with the aim of determining the exact mechanism behind it.
| Materials and Methods | | |
Study design
The PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) guidelines were followed when conducting and reporting this systematic review. The patient population examined included athletic participants who either suffered a concussion, LEI, or both. Our primary outcome measure was LEI rates after a complete return to play following concussion. There were no restrictions placed on follow-up duration. Studies written in English as well as peer-reviewed studies were used as eligibility criteria.
Search strategy
A medical center librarian was consulted during the design phase of the search process. The electronic databases PubMed, CINAHL, Embase, and SPORTDiscus were used to identify studies from all time periods available in the respective electronic databases. A search query related to concussion and injury was compiled from keywords and controlled vocabulary for each database. The PubMed search query can be found below in the Appendix. In addition, reference lists of relevant articles were hand searched after the electronic database search in order to ensure all articles of interest were included. The database and hand search strategy used to collect all relevant articles was completed on March 14, 2017 [Appendix].
Study selection
From the total of 459 articles, 376 nonduplicate titles and abstracts were retained for initial review. A filter was used to ensure only peer-reviewed English-language articles were included. Two reviewers performed a two-step process to review titles and abstracts for relevance with the following inclusion/exclusion criteria: (1) sports-related activities (i.e., all sports and athletic participation), (2) population (athletic participants, no age or gender exclusion), and (3) outcomes (those who suffered a concussion, a LEI, or both). Full-text documents identified by either reviewer were then collected for further examination by both reviewers. Upon a thorough review, both reviewers had to agree an included article could remain in the study based on the Downs and Black Criteria (see below). In the event both primary reviewers disagreed, a third reviewer completed an independent review to adjudicate the decision to retain or remove a selected article. In addition to the database search of articles, reference lists of relevant articles were hand searched and screened using the methods described above between the two reviewers to ensure that all articles of relevance were included in the review. A summary of the PRISMA flow literature search is shown in [Figure 1].
Assessment of study quality and level of evidence
A modified Downs and Black[39] questionnaire was used to assess the methodological quality of the included studies. The checklist includes criteria that were relevant to assessing potential sources of bias in the included studies [Table 1]. There is a lower risk of bias in the study if more items are satisfied in this assessment. Two authors (JB and TS) independently assessed each study and any disagreements were adjudicated by a third-party reviewer (MF). Each study had the potential to maximally score 28 points based on the Downs and Black scale[40] (however, questions 4, 8, 14, 15, 19, 23, 24, and 27 were not applicable to the study type included in this systematic review and were not scored. This brought the modified Downs and Black maximum score to 20. The Oxford Centre for Evidence Based Medicine “Levels of Evidence 1,” document was used to rate the level of evidence for each study included in the systematic review. The results of these assessments can be found in [Table 1]. | Table 1: Modified Downs and Black Checklist and Oxford Center of Evidence Based Medicine Analysis
Click here to view |
| Review Results | | |
The search yielded 454 results from the database search, as well as five additional hand searched articles, with a total yield of 459. Of the original database search, 376 articles were identified using our PRISMA criteria. Of the 376 articles, 101 passed the title screening and moved on to abstract review. Thirteen articles moved on to full-text review after abstract review and assessed for inclusion eligibility. At the conclusion of the text review, ten studies ultimately met the study inclusion criteria, identified from the initial database search.
Risk results
The risk of LEI following a concussion ranged in studies with odds ratios ranging from 1.72 to 2.48, hazards ratios ranging from 1.47 to 4.07, and the incident rate ratio ranging from 1.97 to 2.02 in athletes who had acquired a concussion versus those who did not. One study did not use a control group and an association between.
Summary of included studies
A summary of the ten studies included in the systematic review is presented in [Table 2].
Overall, eight of the ten studies meeting the inclusion criteria demonstrated a link between concussion and LEI.[4],[10],[11],[12],[13],[35],[37],[38] In total, 7784 athletic participants were analyzed for increased LEI risk across studies. The studies included a wide age range of athletes (mean age = 25); both male (89.5%) and female (10.5%) participants; multiple sports (soccer, Australian rules soccer, football, rugby, ice hockey, lacrosse, basketball, handball, floor ball, volleyball, softball, and wrestling), and varying levels of play (amateur to professional). The large number of athletes as well as the wide range of sports suggests the results are not limited to certain populations or participants.
The Downs and Black Checklist[39] was used to assess study quality, assigning each question answered “Y” which indicates a “Yes,” a value of 1 point (except in the case of question five where a “Yes” could be 2 or 1 based on full of partially reported values respectively), and every “N” response indicating “No” is assigned a value of 0. Score ranges were given corresponding quality levels as previously reported;[40] excellent (26–28); good (20–25); fair (15–19); and poor (≤14). It is worth noting that a total score of 20 was the maximum based on the modified version of the Downs and Black[40] used in this analysis. This subset of questions was applicable to the cohort studies used in this review. Taken together, the maximum grade that could be given to a study in our review was “good.” Based on these score ranges, three studies had quality score levels in the “good” scoring range (20–25),[10],[35],[36] six scored in the fair scoring range (15–19)[4],[11],[12],[14],[37],[38] and one study scored in the “poor” scoring range (≤14).[13] Taken together, this means that seven of the eight studied that found a significant association between concussions and LEI risk scored in the “fair” or “good” scoring range.[4],[10],[11],[12],[35],[37],[38] An assessment of level of evidence based on the Oxford Centre for Evidence-based Medicine – Levels of Evidence analysis indicates that all ten studies have a level of 2b evidence, as all were individual cohort studies.
It is worth noting the inconsistent follow-up period between the studies included in this review. One of the studies[14] tracked injuries for 7, 21, and 42 days. They concluded that players sustaining one concussion were not at greater risk for a subsequent LEI compared to their control group (knee-injured athletes) during this shorter follow-up period (s). Four studies included the same follow-up injury-tracking period of 90 days.[10],[11],[37],[38] Three of these studies found an increased injury risk during this time period.[11],[37],[38] Lynall et al.,[10] did not find an increased risk through the first 90 days, but did reveal an increased risk through 180 and 365 days.
| Discussion | | |
The most important finding indicated through this systematic review is that there appears to be an association between sports-related concussion and increased risk of lower limb injury in the weeks to months that follow return to activity. These results should be interpreted with caution as there may be many confounding factors playing into this association such as style of play and playing position. Nevertheless, this review highlights the need for additional research to focus on subtle impairments that may be leaving concussed athletes predisposed to lower extremity injuries. The majority of studies (eight out of ten) meeting the inclusion and exclusion criteria indicate an association between concussion and LEI risk following return to sport.[4],[10],[11],[12],[13],[35],[37],[38] Of the studies indicating an association between concussion and LEI, seven studies scored in the “good” to “fair” scoring range on the modified Downs and Black checklist,[39] indicating a sufficient quality of evidence, even when considering the modified version of the checklist was used. Sports-related concussions remain a significant health concern for active individuals. Postconcussion problems are noteworthy and as stated previously, include issues related to neurocognitive performance, psychological issues, and the potential for a second concussion. In addition to these health concerns, recent evidence has indicated that individuals are also at risk for suffering a LEI following return-to-sport.[4],[10],[11],[12],[13],[35],[37],[38] The primary goal of this systematic review was to present the current information examining LEI risk following concussion. This finding met our hypothesis that there is sufficient high-quality evidence indicating an association between concussion and increased LEI risk following return to activity. There is mounting evidence sufficient to establish a need for future research determining if return-to-sport guidelines should include screening for LEI risk and determining the specific mechanism by which LEI risk is increased. The studies we ultimately included represented a wide range of sports; a relatively wide age range; males and females; and both amateur and professional athletes. Each of these studies included either a separate control group[4],[10],[13],[14],[36],[37],[38] or a within-group analysis, comparing the concussion group to themselves,[12] or both.[11],[35] The risk of LEI ranged from 1.56 to 4.07 times more depending on the study [Table 2]; although, comparisons across studies were complicated due to varying postconcussion follow-up periods during which LEIs were tracked.
It is difficult to make conclusions on when individuals are at increased injury risk following concussion due to the inconsistent postconcussion follow-up time periods. One of the studies[14] tracked injuries for 7, 21, and 42 days. They concluded that players sustaining one concussion were not at greater risk for a subsequent LEI compared to their control group (knee-injured athletes) during this shorter follow-up period(s). The strongest evidence for increased LEI risk comes from the four studies that included the same follow-up injury-tracking period (90 days).[10],[11],[37],[38] Three of these studies found an increased injury risk during this time period.[11],[37],[38] Lynall et al.[10] did not find an increased risk through the first 90 days, but did reveal an increased risk through 180 and 365 days. Injury epidemiology studies employing consistent follow-up time periods will enhance our ability to measure true LEI risk following concussion to better understand this link.
Two of the ten articles included in this review did not show a significant relationship between concussion and subsequent LEI.[14],[36] The reason for these contradictory results may be based on methodological considerations. Makdissi et al.[36] experienced a Type II error in their results and failed to reject the null hypothesis due to a small sample size found in the concussed group. Nyberg et al.,[14] did not employ a truly uninjured control group. Instead, their control group included athletes who had suffered an orthopedic knee injury. They attempted to determine if concussion placed athletes at greater risk for subsequent LEI compared to knee-injured players. The fact that they used a knee-injured group as a control group complicates comparisons to the other studies included in this systematic review as all other studies used healthy control subjects. In addition, Nyberg et al.[14] discussed their small sample size as the main limitation to their study.
The main finding of this study indicates that there is an association between concussion and subsequent risk of LEI. This finding suggests there is a need to determine the mechanism by which LEI risk is increased. Maintaining functional joint stability is a complex process often altered by neurological injury such as a concussion. Previous research has demonstrated persistent changes in motor control and neuromuscular function;[10],[11],[12],[13],[14] postural stability;[16],[17],[18],[19],[20] performance of dual-tasks such as gait with added cognitive load;[20],[21],[22],[23],[24],[25],[26] and strength[27],[28] following concussion. Several recent studies may provide some insight into the effect of concussion on functional joint stability.[41],[42],[43] For example, Lapointe et al.[41] examined joint kinematics during a jump cut motion in young adults with a concussion history. Individuals with a concussion history demonstrated less knee varus and knee external rotation, which the authors indicated placed them into a position of knee valgus and knee internal rotation, potentially a more dangerous cutting motion. Howell et al.[42] recently observed persistent deficits while postconcussion individuals performed a dual-task with gait – taking longer to perform the task compared to healthy, matched controls. Finally, Reed et al.[43] examined youth hockey players who had suffered a concussion. They determined that concussed players had lower strength and poorer jump height performance following concussion compared to controls. The mechanism by which concussion is associated with and potentially increases the risk for LEI remains unknown but warrants continued research.
| Conclusion | | |
The results of this systematic review indicate that there is high-quality evidence suggesting an association between concussion and subsequent LEI risks. Although the majority of the studies in this systematic review link concussion with subsequent LEI risk, further research is necessary to determine when this risk is increased and if this risk can be reduced with appropriate postconcussion care. These further studies should focus on creating a better proportion of individuals based on gender, as well as looking into risks associated with both contact and noncontact sports and if the risk of LEI holds up in both cases when you separate sports based on this. This likely will require research examining the causal link between concussion and LEI to determine the mechanism increasing LEI risk, as well as the development of screening tools to identify individuals at risk for LEI.
Clinical significance
In active individuals who have suffered a concussion, even after acute symptoms resolve, the long-term consequences and cognitive deficits that persist remain a pervasive topic of study in sports medicine research. Recently, there have been numerous studies reporting increased risks of lower extremity injuries following return to activity even after symptoms are no longer present. This suggests that the current return-to-activity guidelines following a concussion may not be sensitive enough to detect changes that predispose an individual to lower extremity injuries.
Acknowledgments
There was no source of funding or additional support when conducting this literature review.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
Appendix
Search Terms used in this review: PubMed
(((”Brain concussion”[mesh] OR “Concussion”[tiab] OR “concussions”[tiab] OR “concussed”[tiab] OR “Postconcussive”[tiab] OR “brain injury”[tiab] OR “brain injuries”[tiab]) AND (”Sports”[Mesh] OR “Sport”[tiab] OR “Athletes”[Mesh] OR “athlete”[tiab] OR “athletic”[tiab] OR “football”[Mesh] OR “soccer”[Mesh] OR “hockey”[Mesh] OR “rugby”[tiab] OR “baseball”[Mesh] OR “softball”[tiab] OR “gymnastics”[Mesh] OR “Boxing”[Mesh] OR “football”[tiab] OR “soccer”[tiab] OR “hockey”[tiab] OR “baseball”[tiab] OR “gymnastics”[tiab] OR “Boxing”[tiab]) AND (”Lower Extremity”[Mesh] OR “lower extremity”[tiab] OR “lower extremities”[tiab] OR “Buttocks”[Mesh] OR “buttocks”[tiab] OR “buttock”[tiab] OR “Foot”[Mesh] OR “foot”[tiab] OR “feet”[tiab] OR “Ankle Joint”[Mesh] OR “Ankle”[Mesh] OR “ankle”[tiab] OR “heel”[Mesh] OR “heels”[tiab] OR “Hip”[Mesh] OR “hip”[tiab] OR “hips”[tiab] OR “knee”[Mesh] OR “knee”[tiab] OR “knees”[tiab] OR “Leg”[Mesh] OR “Leg”[tiab] OR “legs”[tiab] OR “thigh”[Mesh] OR “thigh”[tiab] OR “thighs”[tiab] OR “toes”[mesh] OR “toe”[tiab] OR “toes”[tiab] OR “tibia”[Mesh] OR “tibia”[tiab] OR “femur”[Mesh] OR “femur”[tiab] OR “hamstring”[tiab] OR “hamstrings”[tiab] OR “Posterior Cruciate Ligament”[Mesh] OR “Ligament”[tiab] OR “Ligaments”[tiab] OR “Anterior Cruciate Ligament”[Mesh] OR “Patellar Ligament”[Mesh] OR “Medial Collateral Ligament, Knee”[Mesh] OR “Menisci, Tibial”[Mesh] OR “meniscus”[tiab] OR “Pelvis”[Mesh] OR “pelvis”[tiab] OR “pelvic”[tiab]) AND (”Injuries”[subheading] OR “Athletic injuries”[mesh] OR “Injury”[tiab] OR “injuries”[tiab] OR “Leg Injuries”[Mesh] OR “Ankle Injuries”[Mesh] OR “Femoral Fractures”[Mesh] OR “Foot Injuries”[Mesh] OR “Knee Injuries”[Mesh] OR “Medial Tibial Stress Syndrome”[Mesh] OR “Tibial Fractures”[Mesh] OR “Sprains and Strains”[Mesh] OR “sprains”[tiab] Or “sprain”[tiab] OR “Tendon Injuries”[Mesh] OR “Tendinopathy”[Mesh] OR “Tendinopathy”[tiab] OR “ankle fractures”[Mesh] OR “fractures”[tiab] OR “fracture”[tiab]))) AND ((randomized controlled trial[pt] OR controlled clinical trial[pt] OR randomized[tiab] OR randomized[tiab] OR randomization[tiab] OR randomization[tiab] OR placebo[tiab] OR drug therapy[sh] OR randomly[tiab] OR trial[tiab] OR groups[tiab] OR Clinical trial[pt] OR “clinical trial”[tiab] OR “clinical trials”[tiab] OR “evaluation studies”[Publication Type] OR “evaluation studies as topic”[MeSH Terms] OR “evaluation study”[tiab] OR evaluation studies[tiab] OR “intervention studies”[tiab] OR “intervention study”[tiab] OR “intervention studies”[tiab] OR “case-control studies”[MeSH Terms] OR “case-control”[tiab] OR “cohort studies”[MeSH Terms] OR cohort[tiab] OR “longitudinal studies”[MeSH Terms] OR “longitudinal”[tiab] OR longitudinally[tiab] OR “prospective”[tiab] OR prospectively[tiab] OR “retrospective studies”[MeSH Terms] OR “retrospective”[tiab] OR “follow up”[tiab] OR “comparative study”[Publication Type] OR “comparative study”[tiab] OR systematic[subset] OR “meta-analysis”[Publication Type] OR “meta-analysis as topic”[MeSH Terms] OR “meta-analysis”[tiab] OR “meta-analyses”[tiab]) NOT (Editorial[ptyp] OR Letter[ptyp] OR Case Reports[ptyp] OR Comment[ptyp]) NOT (animals[mh] NOT humans[mh]))
| References | | |
| 1. | Langlois JA, Rutland-Brown W, Wald MM. The epidemiology and impact of traumatic brain injury: A brief overview. J Head Trauma Rehabil 2006;21:375-8.  |
| 2. | Marin JR, Weaver MD, Yealy DM, Mannix RC. Trends in visits for traumatic brain injury to emergency departments in the United States. JAMA 2014;311:1917-9. |
| 3. | Clark M, Guskiewicz K. Sport-related traumatic brain injury. Frontiers in Neuroscience. In: Laskowitz D, Grant G, editors. Translational Research in Traumatic Brain Injury. Boca Raton (FL): CRC Press/Taylor and Francis Group; 2016. Available from: http://www.ncbi.nlm.nih.gov/books/NBK326721/. [Last cited on 2018 Jun 05]. |
| 4. | Cross M, Kemp S, Smith A, Trewartha G, Stokes K. Professional Rugby Union players have a 60% greater risk of time loss injury after concussion: A 2-season prospective study of clinical outcomes. Br J Sports Med 2016;50:926-31. |
| 5. | Lovell MR, Solomon GS. Neurocognitive test performance and symptom reporting in cheerleaders with concussions. J Pediatr 2013;163:1192-50. |
| 6. | Ellemberg D, Leclerc S, Couture S, Daigle C. Prolonged neuropsychological impairments following a first concussion in female university soccer athletes. Clin J Sport Med 2007;17:369-74. |
| 7. | Guskiewicz KM, Marshall SW, Bailes J, McCrea M, Harding HP Jr, Matthews A, et al. Recurrent concussion and risk of depression in retired professional football players. Med Sci Sports Exerc 2007;39:903-9. |
| 8. | Didehbani N, Munro Cullum C, Mansinghani S, Conover H, Hart J Jr., Depressive symptoms and concussions in aging retired NFL players. Arch Clin Neuropsychol 2013;28:418-24. |
| 9. | Cantu RC. Recurrent athletic head injury: Risks and when to retire. Clin Sports Med 2003;22:593-603, x. |
| 10. | Lynall RC, Mauntel TC, Padua DA, Mihalik JP. Acute lower extremity injury rates increase after concussion in college athletes. Med Sci Sports Exerc 2015;47:2487-92. |
| 11. | Nordström A, Nordström P, Ekstrand J. Sports-related concussion increases the risk of subsequent injury by about 50% in elite male football players. Br J Sports Med 2014;48:1447-50. |
| 12. | Pietrosimone B, Golightly YM, Mihalik JP, Guskiewicz KM. Concussion frequency associates with musculoskeletal injury in retired NFL players. Med Sci Sports Exerc 2015;47:2366-72. |
| 13. | Gilbert FC, Burdette GT, Joyner AB, Llewellyn TA, Buckley TA. Association between concussion and lower extremity injuries in collegiate athletes. Sports Health 2016;8:561-7. |
| 14. | Nyberg G, Mossberg KH, Tegner Y, Lysholm J. Subsequent traumatic injuries after a concussion in elite ice hockey : A study over 28 years. Curr Res Concussion 2015;2:109-12. |
| 15. | Catena RD, van Donkelaar P, Chou LS. The effects of attention capacity on dynamic balance control following concussion. J Neuroeng Rehabil 2011;8:8. |
| 16. | Riemann BL, Guskiewicz KM. Effects of mild head injury on postural stability as measured through clinical balance testing. J Athl Train 2000;35:19-25. |
| 17. | Guskiewicz KM, Ross SE, Marshall SW. Postural stability and neuropsychological deficits after concussion in collegiate athletes. J Athl Train 2001;36:263-73. |
| 18. | Zazulak BT, Hewett TE, Reeves NP, Goldberg B, Cholewicki J. Deficits in neuromuscular control of the trunk predict knee injury risk: A prospective biomechanical-epidemiologic study. Am J Sports Med 2007;35:1123-30. |
| 19. | Sosnoff JJ, Broglio SP, Shin S, Ferrara MS. Previous mild traumatic brain injury and postural-control dynamics. J Athl Train 2011;46:85-91. |
| 20. | Catena RD, van Donkelaar P, Chou LS. Different gait tasks distinguish immediate vs. long-term effects of concussion on balance control. J Neuroeng Rehabil 2009;6:25. |
| 21. | Catena RD, van Donkelaar P, Chou LS. Cognitive task effects on gait stability following concussion. Exp Brain Res 2007;176:23-31. |
| 22. | Howell DR, Osternig LR, Chou LS. Return to activity after concussion affects dual-task gait balance control recovery. Med Sci Sports Exerc 2015;47:673-80. |
| 23. | Parker TM, Osternig LR, Lee HJ, Donkelaar Pv, Chou LS. The effect of divided attention on gait stability following concussion. Clin Biomech (Bristol, Avon) 2005;20:389-95. |
| 24. | Parker TM, Osternig LR, Donkelaar PV, Chou L. Gait stability following concussion. Med Sci Sports Exerc 2006;38:1032-40. |
| 25. | Parker TM, Osternig LR, van Donkelaar P, Chou LS. Recovery of cognitive and dynamic motor function following concussion. Br J Sports Med 2007;41:868-73. |
| 26. | Buckley TA, Munkasy BA, Tapia-Lovler TG, Wikstrom EA. Altered gait termination strategies following a concussion. Gait Posture 2013;38:549-51. |
| 27. | Killington MJ, Mackintosh SF, Ayres M. An isokinetic muscle strengthening program for adults with an acquired brain injury leads to meaningful improvements in physical function. Brain Inj 2010;24:970-7. |
| 28. | Katz-Leurer M, Rotem H, Keren O, Meyer S. The relationship between step variability, muscle strength and functional walking performance in children with post-traumatic brain injury. Gait Posture 2009;29:154-7. |
| 29. | Daniel DM, Malcom LL, Losse G, Stone ML, Sachs R, Burks R. Instrumented measurement of anterior laxity of the knee. J Bone Joint Surg Am 1985;67:720-6. |
| 30. | Lephart SM, Abt JP, Ferris CM. Neuromuscular contributions to anterior cruciate ligament injuries in females. Curr Opin Rheumatol 2002;14:168-73. |
| 31. | McNair PJ, Marshall RN. Landing characteristics in subjects with normal and anterior cruciate ligament deficient knee joints. Arch Phys Med Rehabil 1994;75:584-9. |
| 32. | Riemann BL, Lephart SM. The sensorimotor system, part I: The physiologic basis of functional joint stability. J Athl Train 2002;37:71-9. |
| 33. | Solomonow M, Krogsgaard M. Sensorimotor control of knee stability. A review. Scand J Med Sci Sports 2001;11:64-80. |
| 34. | Ghez C, Krakauer J. The organization of movement. Principles of Neural Science. Sixth Edition. McGraw-Hill. New York City, New York, USA. p. 73. |
| 35. | Burman E, Lysholm J, Shahim P, Malm C, Tegner Y. Concussed athletes are more prone to injury both before and after their index concussion: A data base analysis of 699 concussed contact sports athletes. BMJ Open Sport Exerc Med 2016;2:e000092. |
| 36. | Makdissi M, McCrory P, Ugoni A, Darby D, Brukner P. A prospective study of postconcussive outcomes after return to play in Australian football. Am J Sports Med 2009;37:877-83. |
| 37. | Brooks MA, Peterson K, Biese K, Sanfilippo J, Heiderscheit BC, Bell DR. Concussion increases odds of sustaining a lower extremity musculoskeletal injury after return to play among collegiate athletes. Am J Sports Med 2016;44:742-7. |
| 38. | Herman DC, Jones D, Harrison A, Moser M, Tillman S, Farmer K, et al. Concussion may increase the risk of subsequent lower extremity musculoskeletal injury in collegiate athletes. Sports Med 2017;47:1003-10. |
| 39. | Downs SH, Black N. The feasibility of creating a checklist for the assessment of the methodological quality both of randomised and non-randomised studies of health care interventions. J Epidemiol Community Health 1998;52:377-84. |
| 40. | Hooper P, Jutai JW, Strong G, Russell-Minda E. Age-related macular degeneration and low-vision rehabilitation: A systematic review. Can J Ophthalmol 2008;43:180-7. |
| 41. | Lapointe AP, Nolasco LA, Sosnowski A, Andrews E, Martini DN, Palmieri-Smith RM, et al. Kinematic differences during a jump cut maneuver between individuals with and without a concussion history. Int J Psychophysiol 2018;132:93-8. |
| 42. | Howell DR, Osternig LR, Chou LS. Single-task and dual-task tandem gait test performance after concussion. J Sci Med Sport 2017;20:622-6. |
| 43. | Reed N, Taha T, Monette G, Keightley M. A Preliminary exploration of concussion and strength performance in youth ice hockey players. Int J Sports Med 2016;37:708-13. |
[Figure 1]
[Table 1], [Table 2]
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