
==== Front
Int J Sports Phys Ther
Int J Sports Phys Ther
2159
International Journal of Sports Physical Therapy
2159-2896
NASMI Website: International Journal of Sports Physical Therapy

35949388
36810
10.26603/001c.36810
Systematic Review/Meta-Analysis
The Effect of Concussion History on Lower Extremity Injury Risk in College Athletes: A Systematic Review and Meta-Analysis
https://orcid.org/0000-0003-0795-8951
Ramirez Vanessa 1
McCann Ryan 1
Schussler Eric 1
Martinez Jessica 1
1 Rehabilitation Sciences Old Dominion University https://ror.org/04zjtrb98
Corresponding author: Vanessa Ramirez, MSAT Old Dominion University, Norfolk, Virginia vrami002@odu.edu; 909-465-3702
1 8 2022
2022
17 5 753765
18 10 2021
26 4 2022
© The Author(s)
https://creativecommons.org/licenses/by-nc/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (4.0) which permits non-commercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

Introduction

Collegiate athletes who suffer a concussion may possess prolonged impairments even after clearance for return-to-participation, which may place them at an increased risk of lower extremity injury.

Objective

To conduct a systematic review and meta-analysis of studies examining risk of lower extremity musculoskeletal injury following a concussion in collegiate athletes.

Methods

A literature search was performed using the following databases: PubMed, CINAHL, SPORTDiscus. The following search terms were used to identify relevant articles, [“concussion” OR “brain injury” OR “mild traumatic brain injury” OR “mTBI”] AND [“lower extremity injury” OR “musculoskeletal injury”]. Articles were included if they were published between January 2000 and July 2021 and examined collegiate athletes’ risk of sustaining a lower extremity musculoskeletal injury following a concussion. Methodological quality of included studies was performed with a modified Downs and Black Checklist. The primary outcome of interest was the risk of sustaining a lower extremity musculoskeletal injury following a concussion. A random effects meta-analysis was conducted in which a summative relative risk (RR) for sustaining a lower extremity injury in athletes with and without a history of concussion was calculated.

Results

Seven studies met the eligibility criteria to be included in the systematic review. There were 348 athletes in the concussion group and 482 control athletes in the included studies. Most of the studies were of good or excellent quality. Five of the seven studies were able to be included in the meta-analysis. College athletes who suffered a concussion possessed a 58% greater risk of sustaining a lower extremity musculoskeletal injury than those who did not have a history of a concussion (RR = 1.58[1.30, 1.93]).

Conclusions

Lower extremity injury risk is potentially increased in college athletes following a concussion compared to those without a history of a concussion. Further research is needed to investigate the mechanism behind this increased risk. Clinical assessments throughout the concussion return-to-play protocol may need to be improved in order to detect lingering impairments caused by concussions.

Level of Evidence

1

traumatic brain injury
musculoskeletal injury
==== Body
pmcINTRODUCTION

Sport-related concussion has been defined as a traumatically induced alteration of mental status that may or may not involve loss of consciousness1,2 and usually results in impaired mental status, balance, and delayed reaction time.3 Concussions constitute between 3.65 percent and 13.1 percent of all sport-related injuries that occur while participating in collegiate athletics.4 There is also a percentage of concussions that go unreported and undiagnosed each year. Since a number of concussions go unreported, the true annual incidence is likely 40% higher because college athletes knowingly hide symptoms of their concussion and choose not to report it.5

Many different assessment tools and techniques are used to assess and diagnose a concussion and determine readiness for return-to-play (RTP). Traditional evaluation methods, such as static balance tests, may have limited clinical utility for detecting certain physiological deficits concussion patients experience after RTP.2,6,7 While static and responsive balance control must be restored, many individuals recovering from a concussion display an initial improvement in postural sway during balance assessment, but then regress after RTP.8 Furthermore, college football players who sustained a concussion during a season exhibited decreased knee stiffness with increased hip stiffness when competing in athletic competition compared to those who did not experience a concussion.9 Higher levels of overall leg stiffness leads to increased loading rates, thus increasing the risk for bony injuries such as stress fractures, while too small an amount of stiffness may lead to excessive joint motion, thus increasing the risk for soft tissue injury.10–16 These findings raise concerns that athletes who are still experiencing deficits and impairments after being cleared to return to play from a concussion may be at increased risk of lower extremity injury.

Previous authors have investigated the effects of concussion on lower extremity musculoskeletal injury risk. McPherson et al.17 conducted a systematic review and meta-analysis of studies that have examined the risk of musculoskeletal injury following a concussion in recreational, high school, college, and professional athletes. This research identified that athletes with a concussion had approximately two times greater odds of sustaining a musculoskeletal injury as compared to controls. Reneker et al.18 also conducted a systematic review and meta-analysis of studies that have examined the risk of injury following a concussion in athletes. In both military and athletic populations, the risk of any type of injury following a concussion was approximately 2.5 times higher in individuals with a history of concussion than those without a history of a concussion.18

While these systematic reviews offer valuable insights regarding connections between concussion and subsequent lower extremity injury, they are partially limited by their inclusion of broad spectrums of athletic populations and musculoskeletal injuries. It is difficult to group service members and college athletes into one cohort because individuals in the military setting may experience concussions or injuries from high-explosive blast forces,18 which is not an environment college athletes are exposed to. Prolonged military operations and exposure to improvised explosive devices (IEDs) blasts have led to significant increases in the incidence and prevalence of concussion in service members.19 Concussions were a predominant injury of the military operations in Iraq and Afghanistan, and the majority were blast related.20 A focus on a narrower patient population, such as collegiate athletes, would allow for a potentially more targeted application of findings clinically. Additionally, because neuromuscular control, sensory processing, and sensory information impairments persist after concussion, risk of subsequent lower extremity injury risk is of particular concern.21–23 Researchers have indicated that neuromuscular impairments occur following a concussion, including impairments in both gait and dynamic postural control.1,24 Thus, the risk of lower extremity injuries following concussion should be specifically examined. A preliminary literature search indicates that since the previous systematic reviews were published, new original research has been published that would support an updated systematic review with a narrower scope. Therefore, the objective of this study was to conduct an updated systematic review examining the risk of lower extremity musculoskeletal injury following a concussion in collegiate athletes.

METHODS

Search Strategy

Guidelines established within the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) statement were followed throughout the review. A literature search was performed using the following databases: PubMed, CINAHL, SPORTDiscus. The following search terms were used to identify relevant articles, [“concussion” OR “brain injury” OR “mild traumatic brain injury” OR “mTBI”] AND [“lower extremity injury” OR “musculoskeletal injury”].

Selection Criteria

The following inclusion criteria was applied:

Prospective studies examining lower extremity injuries in populations with a previous concussion;

Study population consisting of college athletes;

Studies that calculated odds, risk, and/or ratio of sustaining a lower extremity injury after a concussion;

Studies published between January 2000 and July 2021;

Studies published in English;

The following exclusion criteria was applied:

Review articles.

A hand search of articles was performed to find additional eligible studies. References lists of included studies were reviewed.

Article Selection

To determine which articles were to be included in the systematic review, two authors reviewed the article titles and eliminated those that had no relevance to concussion or lower extremity injury. The reviewers then screened the remaining abstracts and eliminated articles that were irrelevant to the systematic review’s topic. Remaining studies’ full text were read and assessed by both investigators, and those that met the inclusion criteria were included in the systematic review. In the case reviewers did not agree, a consensus was reached through discussion. If a consensus was not made, a third reviewer provided the tiebreaker.

Quality Assessment

Included studies were assessed for methodological quality using the Downs and Black Checklist.25 The Downs and Black Checklist was modified prior to quality assessment to eliminate items that were irrelevant to studies within the selection criteria. Items pertaining to study bias and internal and confounding bias, such as items 8 and 16, were removed. Additionally, items referring to follow-up, patient compliance, randomization, and blinding, including items 9, 14, 15, 19, 23, and 26, were removed. The maximum score of the modified Downs and Black Checklist was 19. All studies were assessed independently by two reviewers. In the case reviewers did not agree on initial rankings, a consensus was reached through discussion. If a consensus was not made, a third reviewer provided the tiebreaker.

Data Extraction

Sample sizes, participant demographics, participant inclusion and exclusion criteria, quantities of concussion and lower extremity injury cases, length of injury tracking period, and primary results were extracted from each study. Data were extracted regarding the risk of sustaining a lower extremity musculoskeletal injury following a concussion.

Meta-Analysis

Review Manager software (RevMan, v 5.3; The Nordic Cochrane Center, The Cochrane Collaboration, 2014) was used to perform the meta-analysis. A random-effects meta-analysis produced a pooled relative risk (RR) calculation and 95% confidence interval (CI) that represented the overall results for the studies that provided data that allowed for calculation of relative risk. The relative risk was calculated by using the following formula:

[(number of individuals with a history of concussion who suffered a lower extremity injury/total number of individuals with a history of concussion)/(number of individuals who suffered a lower extremity injury without a history of a concussion/total number of individuals without a history of concussion)].

A relative risk value greater than one indicates that the odds of an athlete suffering a lower extremity musculoskeletal injury with a history of concussion is greater compared to those athletes with no history of concussion.26 A relative risk value less than one indicates that the odds of an athlete suffering a lower extremity musculoskeletal injury with a history of concussion is lower compared to those athletes with no history of concussion.26 The 95 percent CIs were used to determine the statistical significance of the difference in risk; if the CI crosses one, then it is not considered statistically significant. Heterogeneity of studies included in the meta-analysis was examined using the Q statistic. If the Q statistic was found to be significant, study variables that could potentially introduce heterogeneity were further analyzed. No further analysis was conducted if the Q statistic was not found to be significant. The study variable that was analyzed was the injury tracking timeline. The injury tracking timelines took place within the first 90 days of RTP and after one year of RTP.

RESULTS

A total of 2,873 studies were identified in the initial database search. The hand search process did not yield any additional results. Duplicates were removed and 2,644 articles were identified for assessment of the title. Following removal of articles with titles that had no relevance or concussion or lower extremity injury, 27 articles remained. Once abstracts and full texts were reviewed by the two authors, seven articles met the inclusion criteria for the systematic review. With the application of inclusion and exclusion criteria, seven eligible studies were included in the systematic review. Results of the literature search are shown in Figure 1. Study characteristics are reported in Table 1.

93618 Figure 1. Article selection, following PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) flow diagram.

Quality Assessment

The scores of quality assessment of the included articles ranged from 11 to 18, with five27–31 of the studies scoring 15, 17, or 18. Scores between 16 and 19 were considered excellent quality, scores between 12 and 15 were considered good quality, scores between nine and 11 were considered fair quality, and scores less than nine were considered poor quality. These scores indicate that most of the studies were of good or excellent quality. Some of the reasons for the high-quality scores include clearly describing the study objective, outcome measures, and results, providing the actual probability values, choosing individuals who were representative of the desired population, and matching individuals to controls of the same population. Even though healthy, non-concussed controls were matched for potential confounding factors (i.e., sex, sports, position) in five studies,27–31 two27,28 reported that exposure levels may have not been the same between the concussed athlete group and the matched controls. Sample sizes of the concussed athlete group ranged between studies, ranging from 1227 to 36432 athletes.

Demographic Data

Participants in two28,30 studies were of one sex. Of the remaining five studies, four27–29,33 provided a sex breakdown of the two groups. Of those studies, there were 265 male and 83 female athletes in the concussion groups while there were 349 male and 133 female athletes in the control groups.27–29,33 Sport and participation levels for each study are included in Table 1. Six27–32 studies provided the sports in which the athletes from the concussion group participated. Not all sports were analyzed amongst the studies; the sports frequently investigated were football, men’s and women’s soccer, men’s and women’s basketball, and swimming. Other sports investigated include hockey, wrestling, volleyball, baseball, softball, tennis, cheerleading, golf, field hockey, and rowing. Control athletes, when implemented, were matched by sport and sex. Some studies matched athletes by exposure and position as well.27,28,31,32 Lynall et al.32 further matched concussed athletes to control athletes by age, height, and weight. As for the lower extremity injury time tracking period following concussion, three studies27–29 tracked concussion patients for 90 days after their concussion, one32 reviewed the injury history of the concussed individuals until the end of their intercollegiate athletic career, and another study31 looked at the time before and after 90 days, 180 days, and 365 days of the concussion.

Individual Study Results

Overall, there was a wide variety of inclusion and exclusion criteria for classifying musculoskeletal injuries. The variability of classification of lower extremity injuries amongst the studies may contribute to the different relative risk and results of each. Herman et al.29 found that the odds of sustaining a lower extremity musculoskeletal injury were 3.39 times higher in concussed college athletes, which was the largest odds ratio of all the studies investigated. Two studies30,31 found that individuals with a history of a concussion displayed higher lower extremity injury rates than the control group after 365 days following RTP from a concussion. It was shown that individuals with a history of a concussion were at increased risk of lower extremity musculoskeletal injury27,28,33; and the odds of sustaining a lower extremity injury during the first 90 days of RTP were 2.48 times higher in individuals with a history of concussion compared to those with a history of concussion.27 Furthermore, the odds of experiencing a lower extremity injury were 3.00 times higher in individuals with a history of multiple concussions compared to individuals with a history of a single concussion or no concussion history at all.32

93619 Table 1. Study Characteristics

Authors	Concussed Athletes	Control Athletes	Quality (Downs and Black)	Inclusion Criteria	Exclusion Criteria	Inclusion Criteria for MSK Injury	Exclusion Criteria for MSK Injury	Results	
Brooks et al., 2016	75 (58 male, 17 female)	182 (136 male, 46 female)	17/19	1) All athletes who sustained a concussion during athletic play were diagnosed with a concussion by a team physician 2) athletes who participated in games and practices for a minimum of 72 days (80%) of the 90-day period after RTP 3) athletes with complete medical records regarding diagnosis and RTP date	1) If athletes sustained a second concussion within the 90-day period after RTP 2) if a non-MSK injury, an UE injury, or illness was sustained that limited their sport participation for greater than 18 days (20%) of the 90-day period; 19 cases of concussion excluded	As non-contact acute fractures, muscle strains/tears, or ligament sprains or ruptures of the hip, groin, thigh, knee, shin, ankle, or foot	Contusion, stress fracture, abrasion, overuse injury, and other non-MSK injury	Incidence rate of MSK injury during 90-day period after RTP was higher in concussed athletes (17%) compared with matched controls (9%). Odds of sustaining a LE MSK injury were 2.48 times higher in concussed athletes than in controls	
Fino et al., 2019	110 (76 male, 34 female)	110 (76 male, 34 female)	18/19	Concussion initially suspected by an athletic trainer and later diagnosed by a team physician	Previous concussion within 2 years, subsequent concussion within 365 days, incomplete medical record, or discontinued participation on athletic team; 46 cases excluded	Any acute injury (sprain, strain, contusion, or unspecified acute pain of the LE that required medical attention and were documented in the athlete’s electronic medical record; Included LE injuries in the 365 days preceding concussion and 365 days after concussion	None	Concussed group had a 67% greater relative risk of LE injury compared with controls after adjusting for presence of a previous LE injury	
Harada et al., 2019	48 multiple concussion cases, 48 single concussion cases (all male)	48 male	16/19	MC were defined as any athlete sustaining 2 or more concussion in collegiate career	If athletes had incomplete roster or injury information	Not specified	Not specified	Athletes with MC were found to have a significantly greater odds of LE injury and shorter time to LE injury than matched SC and NC controls	
Herman et al., 2017	73 (52 male, 21 female)	148 (106 male, 42 female)	15/19	Athletes with an in-season concussion as diagnosed by the university primary care sports medicine-certified physician assigned to each athlete’s sport team	1) If they had a history of concussion within the prior 6 months, 2) the concussion occurred outside the competitive season, 3) player had time loss within 30 days of RTP because of issues unrelated to a MSK injury (suspension) or 4) the duration of the remaining competitive season at the time of RTP from a concussion was <30 days	Time loss injury (athlete being withheld from competition for at least 1 day); defined as a strain, sprain, dislocation, or rupture	Overuse injuries, fractures, or contusions	Concussed athletes had a 3.39 times greater risk of muscle strains or tears or ligament sprains/ ruptures in the 90-day period after RTP	
Lynall et al., 2015	44	58	17/19	Concussion diagnosed by the university’s sports medicine staff	If concussion resulted in any positive imaging findings, if participant was admitted to the hospital, if participants sustained a previous concussion while at the university, if no appropriate matched control could be identified, or if there were incomplete notes in the athlete’s medical record	Any injury recorded by a certified AT or team physician in the athlete’s medical record	Not stated	College athletes are almost twice as likely to suffer an acute LE MSK injury after concussion	
Krill et al., 2018	12	25	15/19	Not stated	Not stated	1) Occurred as a result of participation in an organized intercollegiate practice or contest, 2) required medical attention by a team certified athletic trainer or physician, and 3) resulted in restriction of the student-athlete’s participation or performance for > or equal to 1 calendar day beyond the day of injury; included contusion, strain, sprain, stinger or brachial plexopathy, dislocation, or rupture	Not stated	Not a clear increase in LE injury after an athlete sustains a concussion. However, there was an overall increase in the post-concussion group’s LE injury rate for the time period beyond 12 months after a concussion was sustained compared with the control group	
Murray et al., 2020	42 (31 male, 11 female)	42 (31 male, 11 female)	13/19	Athletes with complete and available medical records with a history of a medically diagnosed concussion	If athlete possessed any self-reported vestibular, metabolic, or neurologic condition (excluding concussion), chronic injury that may have caused an individual to miss at least 3 months of sport play, preexisting condition, or a severe LE injury that permanently affected the ability to perform upright static stance	Soft tissue injury or a fracture to the hip, groin, thigh, knee, lower leg, ankle, or foot area	Chronic injury, contusion, abrasion, and laceration	The association between concussion history and injury incidence was significant and resulted in a relative risk of 1.88 for a lower extremity injury in individuals with a history of a concussion	
MSK = musculoskeletal

RTP = return-to-play

UE = upper extremity

LE = lower extremity

NC = no concussion

SC = single concussion

MC = multiple concussions

AT = athletic trainer

Meta-Analysis

Meta-analysis of relative risk was performed using five27–30,32 of the seven studies. In the studies that provided sufficient information to perform calculations, the risk of athletes sustaining a lower extremity musculoskeletal injury after a concussion was compared with athletes sustaining a lower extremity injury who did not have a history of a concussion. Studies were not included in the meta-analysis portion if the data was insufficient for calculating relative risk. Overall, athletes who sustained a concussion had greater risk of lower extremity musculoskeletal injury compared to athletes without a history of a concussion (RR = 1.58[1.30, 1.93]) (Figure 2). Positive tests of heterogeneity were detected within comparisons of injury tracking timelines amongst the studies (Q = 11.46, p = 0.02). Subgroup analysis of injury tracking timelines revealed that the risk of lower extremity injury is particularly elevated within the first 90 days of RTP following a concussion (RR = 2.20[1.58,3.05]), but it is not significantly elevated one year after RTP (RR = 1.26[0.98,1.61]).

93720 Figure 2. Relative risk from individual studies and pooled data from random effects meta-analysis.

DISCUSSION

This systematic review and meta-analysis revealed that individuals are at greater risk of sustaining a lower extremity musculoskeletal injury following a concussion compared to individuals without a history of concussion. College athletes who suffered a concussion possessed a 58% greater risk of sustaining a lower extremity musculoskeletal injury than those who did not have a history of a concussion. The overall duration of this increased risk is unknown, but this risk may last up to one year from injury. The detection of heterogeneity reveals that the small sample of studies varied in their findings. The sub-analysis revealed that college athletes with a history of concussion appear to be at increased risk of lower extremity injury within the first 90 days of RTP, but not at the one-year mark. Injury risk does not appear to remain elevated in spite of evidence that motor impairments persist.34 The neuromuscular control deficits that individuals experience following a concussion may not be as severe, or even present, at the one-year mark compared to during the first 90 days. The ability of the neuromuscular control system to respond to disturbances may improve over time,35 but further research would need to be conducted to verify this hypothesis and determine an average timeline for recovery of these deficits.

These findings suggest that it is important to evaluate these individuals at different time points following RTP. It is not common to re-evaluate individuals who have been cleared to return to sport following a concussion. The findings suggest that re-evaluation may be beneficial and could possibly reduce future injury risk. Even though athletes are no longer experiencing concussion-like symptoms, they may still be experiencing motor abnormalities following return to play. However, these abnormalities may not be detected if the individuals are not re-evaluated.

This systematic review expands on the review performed by McPherson et al.17 by including three additional studies published since the publication of their research. One29 of these studies was included in the current meta-analysis. With the addition of the one study, the meta-analysis revealed similar results to the one performed by McPherson et al.17 Thus, this systematic review further emphasizes that collegiate athletes who have suffered a concussion are at increased risk of lower extremity injury compared to those without a history of concussion.

This meta-analysis strictly examined intercollegiate athletics; whereas the meta-analysis performed by McPherson et al.17 examined professional, recreational, and intercollegiate athletes. The included recreational athletes spanned from 18 to 29 years of age, which may serve as a confounding factor for the increased injury risk. Older individuals generally possess decreased musculoskeletal strength compared to younger individuals, which may serve as a risk factor for future injury.36 On the other hand, an increase in the number of years of experience in a specific sport may reduce an individual’s injury risk because they are an “expert” with better movement patterns and biomechanics.37 The meta-analysis performed in the current study included articles with a specific population, one of strictly college athletes. Since male college athletes were more frequently represented in the included articles, the findings are most applicable to this population. It is difficult to make a determination about the effects of concussion on lower extremity injury risk for males and females of different age groups.

The mechanism behind the increased risk of experiencing a lower extremity musculoskeletal injury is not yet fully understood, but several potential explanations exist. One explanation, which was not assessed with this study, is that a previous history of lower extremity musculoskeletal injury may place these individuals at increased risk of suffering a future injury. It has been shown that previous injury serves as a risk factor for future musculoskeletal injury.38,39 Strength imbalances between muscles have been suggested as risk factors for lower extremity injuries, and may be a consequences of a previous injury.38 Muscle imbalances may affect the efficiency of movements that involve quick accelerations and decelerations, which are common actions in athletics.38

Concussions can involve multiple and varied regions of the brain, including those associated with orienting and executive components of visuospatial attention.40 The regions of the brain that are responsible for these attentional networks include the parietal, frontal, and temporal regions, the cingulate cortices, and the midbrain.41 When one suffers a concussion, these regions may become damaged or impaired, which compromises the ability to process stimuli in terms of disengagement, movement, and re-engagement.42 Even after classic concussion symptoms resolve, there is a possibility that neural and neuromuscular impairments are still present. There is ongoing research in this area that has revealed that individuals continue to experience neuromuscular, neurocognitive, sensory processing, and balance deficits related to concussion well after RTP.

Research has indicated that degradation of neuromuscular control, sensory processing, and sensory information can lead to increased injury risk.31,32 With regions of the brain associated with the executive components of visuospatial attention being most susceptible to damage following a concussion, individuals may possess deficits in processing important information while ignoring extraneous stimuli.35,40 Reduced speed of response to peripheral visual stimuli after concussion may negatively affect anticipatory muscle activation that relies on peripheral visual awareness.43,44 If individuals utilize improper or delayed muscle contractions, they may perform movements that place them in vulnerable positions, which could potentially increase their risk of musculoskeletal injury.

Which specific deficits and how they interact within the individual to increase injury risk has not yet been determined. It has been shown that neuromuscular impairments are risk factors for future injury45,46; and with individuals still experiencing such deficits after return to activity, they may be influential risk factors for sustaining a future musculoskeletal injury.35

Research has shown that individuals still experience lingering gait deficits, including decreased gait speed, cadence, and stride length during dual-task activities following resolution of concussion symptoms.19,47 When these impairments are linked with dual-task conditions, athletes may not be able to coordinate or focus as easily as they were able to prior to their concussion. The addition of a cognitive load may further compound the neurocognitive deficits these individuals already possess and experience. This may lead them to compensatory movement patterns that place stress on body structures that are unable to support this force, and thus make the individual more susceptible to injury. Research indicates that concussed individuals change their gait strategy by spending more time in double-leg stance compared to single-leg stance and possess lower mean gait velocity at 72 hours post-injury compared to non-concussed athletes.48,49 Furthermore, research has shown that individuals with a history of a concussion possess gait abnormalities up to 90 days following a concussion.50,51 With these individuals possessing an altered gait strategy days or weeks after experiencing a concussion, this may serve as a possible indication of the systems of movement that continue to be affected by the injury.

Another possible explanation for the increased injury risk is that individuals with a history of concussion may adopt new movement patterns,22 which may help them “pass” the clinical assessments, such as static balance tasks, in the RTP concussion protocol. It has been suggested that individuals with a history of a concussion maintain upright posture by using more top-down control than bottom-up control compared to individuals without a history.33 Even though the athletes are able to complete the clinical evaluation, it does not necessarily mean that they performed it with the same skill level or motor strategies prior to their concussion. Stride length during gait is significantly shorter for up to 14 days after concussion with a dual-task condition compared to a single-task condition, and gait velocity is significantly slower for up to 28 days post-injury with a dual-task condition compared to a single-task condition.52

Concussed athletes also demonstrate lasting balance impairments following RTP, particularly deficits in dynamic balance48,50,51,53–55 Authors have shown that athletes with a history of a concussion, upon RTP, are able to perform static balance tasks without any difficulty, but struggle to perform dynamic balance tasks.56 Reduced balance performance indicates that an individual is less capable of responding to perturbations and sensing their body’s position in space, potentially leading to mispositioning of the lower extremity. Thus, a balance deficit can place athletes at an increased risk of sustaining an injury. Reduced single-leg balance performance is associated with eight times greater risk of ankle sprain injury.57,58 Returning to baseline values for single-leg balance is an assessment that may not be sensitive enough to detect lingering impairments in concussed athletes.

Future Directions

Healthcare professionals should be aware that collegiate athletes are at increased risk for lower extremity musculoskeletal injury following a concussion, even after being cleared for RTP. Many of the RTP concussion protocol tests are important, but some are subjective, such as the symptom checklist. Research has suggested that current concussion evaluation methods may not possess sufficient sensitivity to detect any lingering concussion-related abnormalities that persist after symptom resolution.59,60 Research should work to identify new methods to evaluate athletes during the RTP concussion protocol to ensure that they are fully prepared to return to their sport and are not experiencing subtle or lingering deficits when returning to participation. It also needs to be determined which lingering deficits or impairments are the cause of this increased risk of injury. If a history of concussion is the factor responsible for increasing the injury risk in these athletes, future research should look to further investigate the neuromuscular changes that are brought about by concussions. Per the sub-analysis findings, it is also important to evaluate college athletes at different time points following RTP after a concussion.

Finally future research can place a larger focus on female collegiate athletes and examine the effect of concussion on lower extremity injury risk on these individuals. Studies can also investigate the effect of concussion in other populations, such as athletes in the secondary school setting and those in recreational or community leagues.

Limitations

This systematic review had a few limitations. Even though the concussed athletes were matched with control groups by sport and position, there are other factors, such as behavior or personality traits of the athletes that could have affected the results.32 If an athlete is more aggressive or partakes in riskier athletic behavior, it may place that athlete at a higher risk of sustaining a musculoskeletal injury.32 Many different sports were explored in each study, thus limiting the ability to draw conclusions regarding the effect of concussion on lower extremity injury risk in specific sports. Not all studies examined athletes of both sexes, making it difficult to make a determination about the effect of concussion on lower extremity injury risk for males and females separately. Another limitation is that the criteria for classifying a lower extremity musculoskeletal injury differed across studies. This could affect the injury risk reported in the included studies, as some studies may have included an injury that another study excluded.

CONCLUSION

The results of this systematic review and meta-analysis indicate that history of a concussion appears to increase the risk of suffering a lower extremity musculoskeletal injury in college athletes. Although not statistically significantly different, following RTP, increased risk is strong at three months post-concussion, but not at one year. Further research is needed to explore and determine the neuromuscular mechanism behind this increased risk of injury and to develop return-to-play criteria that are capable of identifying those at increased risk of lower extremity injury after concussion.

Conflicts of Interest

The authors report no conflicts of interest.
==== Refs
National athletic trainers’ association position statement: management of sport concussion J Athl Train Broglio Steven P. Cantu Robert C. Gioia Gerard A. Guskiewicz Kevin M. Kutcher Jeffrey Palm Michael McLeod Tamara C. Valovich 1 3 2014
49 2 245 265 1062-6050 10.4085/1062-6050-49.1.07 10.4085/1062-6050-49.1.07 24601910
Consensus statement on concussion in sport—the 5thinternational conference on concussion in sport held in Berlin, October 2016 British Journal of Sports Medicine McCrory Paul Meeuwisse Willem Dvorak Jiří Aubry Mark Bailes Julian Broglio Steven Cantu Robert C Cassidy David Echemendia Ruben J Castellani Rudy J Davis Gavin A Ellenbogen Richard Emery Carolyn Engebretsen Lars Feddermann-Demont Nina Giza Christopher C Guskiewicz Kevin M Herring Stanley Iverson Grant L Johnston Karen M Kissick James Kutcher Jeffrey Leddy John J Maddocks David Makdissi Michael Manley Geoff T McCrea Michael Meehan William P Nagahiro Sinji Patricios Jon Putukian Margot Schneider Kathryn J Sills Allen Tator Charles H Turner Michael Vos Pieter E BMJ 26 4 2017
2017;51(11):838-847 bjsports 2017 0306-3674 10.1136/bjsports-2017-097699 10.1136/bjsports-2017-097699
Acute effects and recovery time following concussion in collegiate football players: the NCAA concussion study JAMA McCrea Michael Guskiewicz Kevin M. Marshall Stephen W. Barr William Randolph Christopher Cantu Robert C. Onate James A. Yang Jingzhen Kelly James P. 19 11 2003
290 19 2556 63 0098-7484 10.1001/jama.290.19.2556 10.1001/jama.290.19.2556
Epidemiology of sports-related concussion in NCAA athletes from 2009-2010 to 2013-2014: incidence, recurrence, and mechanisms The American Journal of Sports Medicine Zuckerman Scott L. Kerr Zachary Y. Yengo-Kahn Aaron Wasserman Erin Covassin Tracey Solomon Gary S. 1 9 2015
43 11 2654 2662 0363-5465 10.1177/0363546515599634 10.1177/0363546515599634
Sports-related concussion: anonymous survey of a collegiate cohort Neurology: Clinical Practice Torres D. M. Galetta K. M. Phillips H. W. Dziemianowicz E. M. S. Wilson J. A. Dorman E. S. Laudano E. Galetta S. L. Balcer L. J. 19 7 2013
3 4 279 287 2163-0402 10.1212/cpj.0b013e3182a1ba22 10.1212/cpj.0b013e3182a1ba22 24195017
Diagnosis, prognosis, and clinical management of mild traumatic brain injury The Lancet Neurology Levin Harvey S Diaz-Arrastia Ramon R 5 2015
14 5 506 517 1474-4422 10.1016/s1474-4422(15)00002-2 10.1016/s1474-4422(15)00002-2 25801547
Updated clinical practice guidelines for concussion/mild traumatic brain injury and persistent symptoms Brain Injury Marshall Shawn Bayley Mark McCullagh Scott Velikonja Diana Berrigan Lindsay Ouchterlony Donna Weegar Kelly 14 4 2015
29 6 688 700 0269-9052 10.3109/02699052.2015.1004755 10.3109/02699052.2015.1004755
Longitudinal assessment of balance and gait after concussion and return to play in collegiate athletes J Athl Train Parrington Lucy Fino Peter C. Swanson Clayton W. Murchison Charles F. Chesnutt James King Laurie A. 1 4 2019
54 4 429 438 1062-6050 10.4085/1062-6050-46-18 10.4085/1062-6050-46-18 30933608
Lower extremity stiffness changes after concussion in collegiate football players Med Sci Sport Exer Dubose DOMINIQUE F. Herman DANIEL C. Jones DEBORAH L. TILLMAN SUSAN M. CLUGSTON JAMES R. PASS ANTHONY HERNANDEZ JORGE A. VASILOPOULOS TERRIE HORODYSKI MARYBETH CHMIELEWSKI TERESE L. 1 2017
49 1 167 172 0195-9131 10.1249/mss.0000000000001067 10.1249/mss.0000000000001067 27501359
Relationships between ground reaction force and tibial bone acceleration parameters Int J Sport Biomech Hennig Ewald M. Lafortune Mario A. 8 1991
7 3 303 309 0740-2082 10.1123/ijsb.7.3.303 10.1123/ijsb.7.3.303
Bone mass, external loads, and stress fractures in female runners Int J Sport Biomech Grimston Susan K. Engsberg Jack R. Kloiber Reinhard Hanley David A. 8 1991
7 3 293 302 0740-2082 10.1123/ijsb.7.3.293 10.1123/ijsb.7.3.293
Effect of repetitive impulse loading on the knee joints of rabbits Clin Orthop Radin E.L. Ehrlich M.G. Chernack R. Abernathy P. Paul I.L. Rose R.M. 1978
131 293 299
Bone remodeling in response to in vivo fatigue microdamage Journal of Biomechanics Burr David B. Martin R.Bruce Schaffler Mitchell B. Radin Eric L. 1 1985
18 3 189 200 0021-9290 10.1016/0021-9290(85)90204-0 10.1016/0021-9290(85)90204-0
Gender differences in active musculoskeletal stiffness. Part II. Quantification of leg stiffness during functional hopping tasks Journal of Electromyography and Kinesiology Granata K.P. Padua D.A. Wilson S.E. 4 2002
12 2 127 135 1050-6411 10.1016/s1050-6411(02)00003-2 10.1016/s1050-6411(02)00003-2 11955985
Lower extremity stiffness in runners with different foot types Gait Posture Williams D.S. McClay Davis I. Scholz J.P. Hamill J. Buchanan T.S. 2003

Arch structure and injury patterns in runners Clinical Biomechanics Williams Dorsey S., III McClay Irene S. Hamill Joseph 5 2001
16 4 341 347 0268-0033 10.1016/s0268-0033(01)00005-5 10.1016/s0268-0033(01)00005-5 11358622
Musculoskeletal injury risk after sport-related concussion: a systematic review and meta-analysis The American Journal of Sports Medicine McPherson April L. Nagai Takashi Webster Kate E. Hewett Timothy E. 2019
47 7 1754 1762 0363-5465 10.1177/0363546518785901 10.1177/0363546518785901 30074832
History of concussion and risk of subsequent injury in athletes and service members: a systematic review and meta-analysis Musculoskeletal Science and Practice Reneker Jennifer C. Babl Ryan Flowers Meredith M. 7 2019
42 2 173 185 2468-7812 10.1016/j.msksp.2019.04.004 10.1016/j.msksp.2019.04.004 31014921
Concussion in the military: an evidence-base review of mTBI in US military personnel focused on posttraumatic headache Current Pain and Headache Reports Holtkamp Matthew D Grimes Jamie Ling Geoffrey 15 4 2016
20 6 37 1531-3433 10.1007/s11916-016-0572-x 10.1007/s11916-016-0572-x
Repeated concussion among U.S. military personnel during operation iraqi freedom The Journal of Rehabilitation Research and Development Macgregor Andrew J. Dougherty Amber L. Morrison Rosemary H. Quinn Kimberly H. Galarneau Michael R. 2011
48 10 1269 78 0748-7711 10.1682/jrrd.2011.01.0013 10.1682/jrrd.2011.01.0013 22234670
Altered gait termination strategies following a concussion Gait & Posture Buckley Thomas A. Munkasy Barry A. Tapia-Lovler Tiffen G. Wikstrom Erik A. 7 2013
38 3 549 551 0966-6362 10.1016/j.gaitpost.2013.02.008 10.1016/j.gaitpost.2013.02.008 23489951
The relationship between neurocognitive function and noncontact anterior cruciate ligament injuries The American Journal of Sports Medicine Swanik Charles Buz Covassin Tracey Stearne David J. Schatz Philip SAGE Publications 6 2007
35 6 943 948 0363-5465 10.1177/0363546507299532 10.1177/0363546507299532 17369562
Effect of neurocognition and concussion on musculoskeletal injury risk Current Sports Medicine Reports Herman Daniel C. Zaremski Jason L. Vincent Heather K. Vincent Kevin R. 2015
14 3 194 199 1537-890X 10.1249/jsr.0000000000000157 10.1249/jsr.0000000000000157 25968852
Altered dynamic postural control during gait termination following concussion Gait & Posture Oldham Jessie R. Munkasy Barry A. Evans Kelsey M. Wikstrom Erik A. Buckley Thomas A. 9 2016
49 437 442 0966-6362 10.1016/j.gaitpost.2016.07.327 10.1016/j.gaitpost.2016.07.327 27522565
The feasibility of creating a checklist for the assessment of the methodological quality both of randomised and non-randomised studies of health care interventions Journal of Epidemiology & Community Health Downs S. H. Black N. 1 6 1998
52 6 377 384 0143-005X 10.1136/jech.52.6.377 10.1136/jech.52.6.377 9764259
Measures of effect: Relative risks, odds ratios, risk difference, and ‘number needed to treat’ Kidney International Tripepi G. Jager K.J. Dekker F.W. Wanner C. Zoccali C. 10 2007
72 7 789 791 0085-2538 10.1038/sj.ki.5002432 10.1038/sj.ki.5002432
Concussion increases odds of sustaining a lower extremity musculoskeletal injury after return to play among collegiate athletes The American Journal of Sports Medicine Brooks M. Alison Peterson Kaitlin Biese Kevin Sanfilippo Jennifer Heiderscheit Bryan C. Bell David R. SAGE Publications 19 1 2016
44 3 742 747 0363-5465 10.1177/0363546515622387 10.1177/0363546515622387
Effects of recent concussion and injury history on instantaneous relative risk of lower extremity injury in division I collegiate athletes Clin J Sports Med Fino Peter C. Becker Lauren N. Fino Nora F. Griesemer Brett Goforth Michael Brolinson Per Gunnar 5 2019
29 3 218 223 1050-642X 10.1097/jsm.0000000000000502 10.1097/jsm.0000000000000502
Concussion may increase the risk of subsequent lower extremity musculoskeletal injury in collegiate athletes Sports Medicine Herman Daniel C. Jones Debi Harrison Ashley Moser Michael Tillman Susan Farmer Kevin Pass Anthony Clugston James R. Hernandez Jorge Chmielewski Terese L. 20 8 2016
47 5 1003 1010 0112-1642 10.1007/s40279-016-0607-9 10.1007/s40279-016-0607-9 27544666
Effect of concussions on lower extremity injury rates at a division I collegiate football program Orthopaedic Journal of Sports Medicine Krill Matthew L. Nagelli Christopher Borchers James Krill Michael K. Hewett Timothy E. 1 8 2018
6 8 232596711879055 2325-9671 10.1177/2325967118790552 10.1177/2325967118790552 30151401
Acute lower extremity injury rates increase after concussion in college athletes Med Sci Sports Exerc Lynall ROBERT C. Mauntel TIMOTHY C. Padua DARIN A. Mihalik JASON P. 12 2015
47 12 2487 2492 0195-9131 10.1249/mss.0000000000000716 10.1249/mss.0000000000000716
Multiple concussions increase odds and rate of lower extremity injury in national collegiate Athletic association athletes after return to play The American Journal of Sports Medicine Harada Garrett K. Rugg Caitlin M. Arshi Armin Vail Jeremy Hame Sharon L. SAGE Publications 12 9 2019
47 13 3256 3262 0363-5465 10.1177/0363546519872502 10.1177/0363546519872502
Baseline postural control and lower extremity injury incidence among those with a history of concussion J Athl Train Murray Nicholas Belson Emily Szekely Brian Islas Arthur Cipriani Daniel Lynall Robert C. Buckley Thomas A. Powell Douglas W. Munkasy Barry 1 2 2020
55 2 109 115 1062-6050 10.4085/1062-6050-187-19 10.4085/1062-6050-187-19 31935138
Motor deficits and recovery during the first year following mild closed head injury Brain Injury Heitger Marcus H. Jones Richard D. Dalrymple-Alford John C. Frampton Chris M. Ardagh Michael W. Anderson Tim J. Informa UK Limited 1 2006
20 8 807 824 0269-9052 10.1080/02699050600676354 10.1080/02699050600676354
Neuromuscular control deficits and the risk of subsequent injury after a concussion: a scoping review Sports Medicine Howell David R. Lynall Robert C. Buckley Thomas A. Herman Daniel C. 17 2 2018
48 5 1097 1115 0112-1642 10.1007/s40279-018-0871-y 10.1007/s40279-018-0871-y 29453743
Spinal cord injury in the geriatric population: risk factors, treatment options, and long term-management Geriatric Orthopaedic Surgery & Rehabilitation Ikpeze Tochukwu C. Mesfin Addisu 20 3 2017
8 2 115 118 2151-4593 10.1177/2151458517696680 10.1177/2151458517696680 28540118
A biomechanical comparison between expert and novice manual materials handlers using a multi-joint EMG-assisted optimization musculoskeletal model of the lumbar spine Journal of Biomechanics Gagnon Denis Plamondon André Larivière Christian 9 2016
49 13 2938 2945 0021-9290 10.1016/j.jbiomech.2016.07.009 10.1016/j.jbiomech.2016.07.009 27469898
Intrinsic risk factors for hamstring injuries among soccer players: a prospective cohort study The American Journal of Sports Medicine Engebretsen Anders Hauge Myklebust Grethe Holme Ingar Engebretsen Lars Bahr Roald 24 3 2010
38 6 1147 1153 0363-5465 10.1177/0363546509358381 10.1177/0363546509358381
Association between previous injury and risk factors for future injury in preprofessional ballet and contemporary dancers Clin J Sports Med Kenny Sarah J. Palacios-Derflingher Luz Shi Qian Whittaker Jackie L. Emery Carolyn A. 5 2019
29 3 209 217 1050-642X 10.1097/jsm.0000000000000513 10.1097/jsm.0000000000000513
Tracking the recovery of visuospatial attention deficits in mild traumatic brain injury Brain Halterman Charlene I. Langan Jeanne Drew Anthony Rodriguez Erika Osternig Louis R. Chou Li-Shan Donkelaar Paul van Oxford University Press (OUP) 2006
129 3 747 753 1460-2156 10.1093/brain/awh705 10.1093/brain/awh705 16330498
The attention system of the human brain Annual Review of Neuroscience Posner Michael I. Petersen Steven E. Annual Reviews 3 1990
13 1 25 42 0147-006X 10.1146/annurev.ne.13.030190.000325 10.1146/annurev.ne.13.030190.000325
Cognitive and brain consequences of conflict Neuroimage Fan Jin Flombaum Jonathan I. McCandliss Bruce D. Thomas Kathleen M. Posner Michael I. 1 2003
18 1 42 57 1053-8119 10.1006/nimg.2002.1319 10.1006/nimg.2002.1319
Analysis of central and peripheral vision reaction times in patients with postconcussion visual dysfunction Clin J Sports Med Clark Joseph F. Ellis James K. Burns Timothy M. Childress John M. Divine Jon G. 9 2017
27 5 457 461 1050-642X 10.1097/jsm.0000000000000381 10.1097/jsm.0000000000000381
The persistent influence of concussive injuries on cognitive control and neuroelectric function J Athl Train Moore Robert D. Hillman Charles H. Broglio Steven P. 1 1 2014
49 1 24 35 1062-6050 10.4085/1062-6050-49.1.01 10.4085/1062-6050-49.1.01 24377962
Biomechanics associated with patellofemoral pain and ACL injuries in sports Sports Medicine Weiss Kaitlyn Whatman Chris Springer Science and Business Media LLC 1 7 2015
45 9 1325 1337 0112-1642 10.1007/s40279-015-0353-4 10.1007/s40279-015-0353-4
Neuromuscular risk factors for knee and ankle ligament injuries in male youth soccer players Sports Medicine Read Paul J. Oliver Jon L. De Ste Croix Mark B. A. Myer Gregory D. Lloyd Rhodri S. Springer Science and Business Media LLC 8 2 2016
46 8 1059 1066 0112-1642 10.1007/s40279-016-0479-z 10.1007/s40279-016-0479-z 26856339
Gait and quiet-stance performance among adolescents after concussion-symptom resolution J Athl Train Berkner Justin Meehan William P., III Master Christina L. Howell David R. 1 12 2017
52 12 1089 1095 1062-6050 10.4085/1062-6050-52.11.23 10.4085/1062-6050-52.11.23 29154694
Return to activity after concussion affects dual-task gait balance control recovery Med Sci Sports Exerc Howell DAVID R. Osternig LOUIS R. Chou LI-SHAN 4 2015
47 4 673 680 0195-9131 10.1249/mss.0000000000000462 10.1249/mss.0000000000000462 25100340
The chronic effects of concussion on gait Archives of Physical Medicine and Rehabilitation Martini Douglas N. Sabin Matthew J. DePesa Sarah A. Leal Elisa W. Negrete Tabitha N. Sosnoff Jacob J. Broglio Steven P. 4 2011
92 4 585 589 0003-9993 10.1016/j.apmr.2010.11.029 10.1016/j.apmr.2010.11.029 21440703
Altered balance control following concussion is better detected with an attention test during gait Gait & Posture Catena Robert D. van Donkelaar Paul Chou Li-Shan 3 2007
25 3 406 411 0966-6362 10.1016/j.gaitpost.2006.05.006 10.1016/j.gaitpost.2006.05.006 16787746
Cognitive task effects on gait stability following concussion Experimental Brain Research Catena Robert D. van Donkelaar Paul Chou Li-Shan Springer Science and Business Media LLC 7 7 2006
176 1 23 31 0014-4819 10.1007/s00221-006-0596-2 10.1007/s00221-006-0596-2 16826411
Gait stability following concussion Med Sci Sport Exerc Parker TONYA M. Osternig LOUIS R. Van Donkelaar Paul Chou LI-SHAN 6 2006
38 6 1032 1040 0195-9131 10.1249/01.mss.0000222828.56982.a4 10.1249/01.mss.0000222828.56982.a4
Recurrent concussion and risk of depression in retired professional football players Med Sci Sports Exerc Guskiewicz KEVIN M. Marshall STEPHEN W. Bailes JULIAN MCCREA MICHAEL HARDING HERNDON P. MATTHEWS AMY MIHALIK JOHNA REGISTER CANTU ROBERT C. 6 2007
39 6 903 909 0195-9131 10.1249/mss.0b013e3180383da5 10.1249/mss.0b013e3180383da5 17545878
The effect of divided attention on gait stability following concussion Clinical Biomechanics Parker Tonya M. Osternig Louis R. Lee Heng-Ju Van Donkelaar Paul Chou Li-Shan 5 2005
20 4 389 395 0268-0033 10.1016/j.clinbiomech.2004.12.004 10.1016/j.clinbiomech.2004.12.004 15737446
Recovery of cognitive and dynamic motor function following concussion Br J Sports Med Parker T.M. Osternig L.R. Van Donkelaar P. Chou L.S. 2007
41 12 868 873 17517857
Concussion history and balance performance in adolescent rugby union players Am J Sports Med Matthews M. Johnston W. Bleakley C. M.. 2021
49 5 1348 1354 33729858
Balance as a predictor of ankle injuries in high school basketball players Clinical Journal of Sport Medicine McGuine Timothy A. Greene Joe J. Best Thomas Leverson Glen 10 2000
10 4 239 244 1050-642X 10.1097/00042752-200010000-00003 10.1097/00042752-200010000-00003
Single leg balance test to identify risk of ankle sprains British Journal of Sports Medicine Trojian T H McKeag D B 10 5 2006
40 7 610 613 0306-3674 10.1136/bjsm.2005.024356 10.1136/bjsm.2005.024356 16687483
Time course of clinical and electrophysiological recovery after sport-related concussion Journal of Head Trauma Rehabilitation Prichep Leslie S. McCrea Michael Barr William Powell Matthew Chabot Robert J. 7 2013
28 4 266 273 0885-9701 10.1097/htr.0b013e318247b54e 10.1097/htr.0b013e318247b54e 22588360
Residual alterations of brain electrical activity in clinically asymptomatic concussed individuals: an EEG study Clinical Neurophysiology Teel E.F. Ray W.J. Geronimo A.M. Slobounov S.M. 4 2014
125 4 703 707 1388-2457 10.1016/j.clinph.2013.08.027 10.1016/j.clinph.2013.08.027 24140103
