Context: 

Dynamic balance deficits have been described postconcussion, even after athletes return to play. Lower extremity (LE) musculoskeletal injury rates increase for up to 1 year after concussion, but the long-term musculoskeletal implications of concussion are unclear.

Objective: 

To (1) examine the association of concussion and LE injury histories with osteoarthritis (OA) prevalence in retired National Football League players and (2) examine the association of concussion and LE injury histories with OA prevalence in those ≤55 years of age.

Design: 

Case-control study.

Setting: 

Survey.

Patients or Other Participants: 

We administered the Health Survey of Retired National Football League Players, which collects information about demographics, OA, LE injury, and concussion history.

Main Outcome Measure(s): 

Twelve discrete categories were created based on concussion and LE injury history, ranging from 0 concussions and 0 LE injuries (referent group) to 3+ concussions and 2+ LE injuries. Binomial regression analysis modeled lifetime OA prevalence. Covariates were body mass index, age at the time of the survey, and total years playing professional football.

Results: 

Complete data were available for 2696 participants. Lifetime OA prevalence was smallest in the referent group (21.1%) and largest in the 3+ concussion and 2+ LE group (50.6%; 2.5 times the referent; 95% confidence interval [CI] = 2.1, 3.1). Participants in all concussion groups (1, 2, 3+) who reported a history of 0 LE injuries had a greater OA prevalence than the referent group. When participants were stratified by age, the ≤55 years of age, 3+ concussions, and 2+ LE injuries group prevalence ratio (3.6; 95% CI = 2.7, 5.2) was larger than that of the >55 years of age, 3+ concussions, and 2+ LE injuries group (1.8; 95% CI = 1.3, 2.4) compared with the respective referent groups.

Conclusions: 

Concussion with or without a history of LE injury may be an important moderator of OA. Future researchers should seek to better understand the mechanisms that influence the association among concussion, LE injury, and OA.

Key Points
  • Retired players who described 1 or more concussions, with or without a history of traumatic lower extremity injury, reported a higher prevalence of osteoarthritis than those with no history of concussion.

  • The association was strongest among those 55 years old or younger.

  • Players who sustained multiple concussions had a higher prevalence of osteoarthritis than those with a history of 0 or 1 concussion.

Concussion leads to acute neurocognitive and balance deficits13  that have been reported to resolve within 7 to 10 days,4  although numerous investigators58  have described impairments lasting beyond this time period and well after the athlete has returned to full activity. Gait measures6,911  and virtual-reality postural-control assessments12  indicate lingering impairments in dynamic postural control and locomotor navigation in previously concussed individuals. Persistent postconcussive neuromuscular-control alterations have been hypothesized to contribute to aberrant movement biomechanics or the inability to adequately react to a potentially injurious stimulus, which may increase the risk of a lower extremity (LE) musculoskeletal injury.1317  Furthermore, aberrant movement biomechanics and joint loading have been implicated as potential risk factors in the development of chronic disability and joint degeneration.18,19  Unfortunately, few researchers have explored how concussion, alone or combined with acute LE injury, may be related to the long-term deterioration of joint health.

Aberrant gait biomechanics related to altered neuromuscular control have been implicated in the incidence and progression of osteoarthritis (OA) in the LE joints.18,19  Additionally, traumatic joint injury is among the most predictive factors related to the risk of developing OA.2022  Long-term changes in biomechanics, influenced by the neuromuscular consequences of joint injury and biochemical alterations in joint homeostasis, likely hasten the onset and progression of LE joint OA.23  Furthermore, concussion increases the risk of sustaining an acute LE joint injury13,14  and may contribute to gross changes in LE biomechanics during gait.6,9,24  Gait alterations have been observed when athletes return to play after concussion, but how long these alterations persist after brain injury is unknown. These neuromuscular-control alterations include greater interjoint coordination variability,25  increased propulsive and braking forces during gait termination,9  and greater center-of-mass medial-lateral displacement6  than in nonconcussed control participants. Just as long-term changes in biomechanics may influence OA progression after LE injury, long-term changes in biomechanics due to concussion may also influence OA development. Thus, it is reasonable to suggest that people who have sustained both a concussion and an LE joint injury may be at higher risk of developing LE OA. Individuals who sustain a concussion and an LE injury early in life, both of which may result in the development of aberrant biomechanics, may be at higher risk of developing OA at an early age.

Currently, there is a dearth of information on the association between concussion and LE injury and the development of chronic musculoskeletal diseases such as OA. Understanding how concussion and LE musculoskeletal injury may collectively influence the progression to OA will be important for developing strategies to improve long-term health after athletic injury. Previous investigators have described an increased prevalence of early-onset OA among retired National Football League (NFL) players26  and an association between reported history of concussion and LE injuries.15  Retired professional football players represent a unique and available cohort of athletes who frequently sustain concussions and LE injuries, which allowed us to investigate this association.

Our primary purpose was to examine the association of concussion and LE injury histories with the prevalence of OA in retired NFL players. Our secondary purpose was to examine the association of concussion and LE injury histories with the prevalence of OA in those 55 years of age and younger. We hypothesized that (1) retired NFL players who had sustained more (2 or 3+) concussions during their careers would have a higher prevalence of OA than retired NFL players who had sustained no or fewer concussions (0 or 1) and (2) the prevalence of OA in those aged 55 and younger would be higher among those who had sustained more concussions (2 or 3+) as opposed to those who had sustained no or fewer concussions (0 or 1).

Participants

Participants were part of the Health Survey of Retired NFL Players.27  This ongoing survey, administered by the Center for the Study of Retired Athletes, collects information from retired NFL players to evaluate multiple aspects of health and wellbeing. The initial survey, completed in 2001, was mailed to 3647 former players who retired between 1930 and 2001. The same survey was also sent to new retirees (those who had not yet received the survey) in 2006 (n = 1272), 2009 (n = 876), 2011 (n = 374), and 2012 (n = 364). Thus, the survey was sent to 6533 retired players in total. The survey was mailed to each player 3 times, and any player who did not respond to the paper survey was contacted via phone. Participant consent was implied based on completion of the paper survey or given verbally during phone interviews. Our university's institutional review board approved the study protocol.

Procedures

The Health Survey of Retired NFL Players

This 13-page paper survey collected information about player demographics, playing history (eg, total years of football played, years of football played at various competitive levels, positions played), general medical history, joint-injury history, and overall health status. For each category, information was requested about the participant's status during and after his football career.

Concussions

We collected information about all concussions sustained during the participant's professional football career. First, each participant was asked, “Did you sustain any concussions during your professional career?” If the answer was yes, the participant was asked how many concussions he sustained during his NFL career.

Lower Extremity Musculoskeletal Injury

We asked for the frequency of specific LE injuries sustained throughout the participant's NFL career. Each player was specifically asked to indicate how many total injuries he had incurred in the following categories: (1) medial collateral ligament tear, (2) lateral collateral ligament tear, (3) anterior cruciate ligament tear, (4) posterior cruciate ligament tear, (5) meniscal tear, (6) hamstrings/quadriceps rupture, (7) calf/Achilles rupture, (8) ankle ligament rupture, and (9) ankle/foot fracture.15  The injuries sustained across the 9 categories were summed.

Osteoarthritis

Participants were asked to respond yes or no to the following question: “Have you ever been told by a physician or health professional that you had/have osteoarthritis/degenerative arthritis?”

Covariates

Self-reported height and mass during the last year each participant played in the NFL were used to compute body mass index (BMI). Additionally, we calculated the total number of years each participant played NFL football and his age at the time the survey was completed.

Statistical Analysis

Coding of Variables

The main outcome, lifetime prevalence of OA, was retained as a dichotomous variable (yes/no). We used 2 main exposures, based on the numbers of NFL career concussions and LE injuries. Our first outcome was the number of LE injuries, categorized as 0, 1, or 2+. Our second outcome was the combination of the number of career concussions and LE injuries. Concussion count was categorized as 0, 1, 2, or 3+. This categorization of concussion history followed previous publications15,27  detailing differences in long-term outcomes based on increasing concussion counts. From the concussion and LE variables, 12 discrete categories were created, ranging from individuals with 0 concussions and 0 LE injuries to individuals with 3+ concussions and 2+ LE injuries. The first covariate, BMI while playing, was computed from self-reported height and weight. For the remaining covariates, total NFL years played and current age, we used the raw data.

Models

Binomial regression models were used to model the lifetime prevalence of OA. Prevalence ratios (PRs) compared the lifetime prevalence of OA among groups. Multivariate models controlled for BMI while playing, total years played, and current age. All binomial regression models used Poisson residuals and robust variance estimation.2830  First, we calculated prevalence ratios that used the categorized LE injury count (0, 1, or 2+); 0 LE injuries was the referent group. Second, we calculated PRs that used the second 12-category exposure, which also considered concussion count; the 0 concussion/0 LE group was the referent group. A PR higher than 1 implied that the group had a higher prevalence of OA compared with the referent group, whereas a PR of less than 1 implied that the group had a lower prevalence of OA compared with the referent group. Any PR with a corresponding 95% confidence interval (CI) that did not include 1.00 was considered statistically significant.

Age Stratification

The previously described methods were used to explore any age-related difference in the association of concussion and LE injury history with lifetime prevalence of OA. For this analysis, we stratified respondents by age: ≤55 years and >55 years. We used 55 years as this is the median age at which knee OA is diagnosed in the general US population.31  For the study, we defined players who completed a survey and indicated they were diagnosed with OA at or before age 55 as individuals with early-onset OA.

Sample

Completed surveys were received from 3226 retired NFL players (49.3% response rate). We excluded any participants who did not report a complete concussion history (n = 234) and those who did not report data for all of our injury variables (n = 51) or for a history of OA (n = 8). Finally, we excluded participants with information missing for any of our 3 covariates (n = 237), resulting in a final data set of 2696 participants.

Descriptive Statistics

Overall, 978 participants (36.3%) reported experiencing OA during their lifetime. Of our sample, 40.1% (n = 1082) reported no concussion history, whereas 19.4% (n = 522), 16.3% (n = 440), and 24.2% (n = 652) reported a history of 1, 2, or 3+ concussions, respectively. A total of 15.8% (n = 427) reported 0 concussions and 0 LE injuries, whereas 16.4% (n = 441) reported 3+ concussions and 2+ LE injuries. The mean age of our sample at the time of the survey was 60.8 ± 11.2 years (age range = 24–95 years), although a slight majority of participants were ≤55 years of age (57.9%). Group demographics along with descriptive statistics for each covariate are detailed in Table 1.

Table 1. 

Group Size and Demographic Information

Group Size and Demographic Information
Group Size and Demographic Information

Binomial Regression Models

The lifetime prevalence of OA increased with the number of LE injuries, ranging from 26.1% for 0 to 29.6% for 1 and 44.4% for 2+ LE injuries (Table 2). Although no difference was found in the lifetime prevalence of OA between the 1 and 0 LE injury groups (PR = 1.1; 95% CI = 1.0, 1.4), the lifetime prevalence of OA in the 2+ LE injuries group was 70% higher than that of the 0 LE injuries group (PR = 1.7; 95% CI = 1.5, 1.9). Results were retained in the multivariate model.

Table 2. 

Lifetime Prevalence of Osteoarthritis and Prevalence Ratios Within Each Group of Lower Extremity Injury Counts, Overall and by Age

Lifetime Prevalence of Osteoarthritis and Prevalence Ratios Within Each Group of Lower Extremity Injury Counts, Overall and by Age
Lifetime Prevalence of Osteoarthritis and Prevalence Ratios Within Each Group of Lower Extremity Injury Counts, Overall and by Age

Univariate and multivariate PRs using the 12-category exposure variable are described in Table 3. The lifetime prevalence of OA was smallest in the 0 concussion/0 LE injuries group (21.1%) and largest in the 3+ concussions/2+ LE injuries group (50.6%). Compared with the 0 concussions/0 LE injuries group, the lifetime prevalence of OA was significantly higher in the majority of the other concussion/LE injury groups. Results were retained in the multivariate models. For example, controlling for BMI while playing, NFL years played, and current age, the lifetime prevalence of OA in the 3+ concussions/2+ LE injuries group was 2.5 times (95% CI = 2.1, 3.1) that of the 0 concussions/0 LE injuries group. In addition, multivariate analyses showed that compared with the 0 concussions/0 LE injuries group, the lifetime prevalence of OA was higher among all concussion groups in the absence of LE injuries (1 concussion/0 LE injuries group PR = 1.4; 95% CI = 1.0, 1.9; 2 concussions/0 LE injuries group PR = 1.7; 95% CI = 1.2, 2.4; 3+ concussions/0 LE injuries group PR = 1.7; 95% CI = 1.2, 2.3; Figure).

Table 3. 

Lifetime Prevalence of Osteoarthritis and Prevalence Ratios Within Each Group of Concussion and Lower Extremity Injury Counts

Lifetime Prevalence of Osteoarthritis and Prevalence Ratios Within Each Group of Concussion and Lower Extremity Injury Counts
Lifetime Prevalence of Osteoarthritis and Prevalence Ratios Within Each Group of Concussion and Lower Extremity Injury Counts
Figure. 

Prevalence ratios for all respondents in each concussion group (1, 2, or 3+ concussions) who reported a history of 0 lower extremity injuries as compared with the referent group (0 concussions, 0 lower extremity injuries). The prevalence of osteoarthritis in all concussion groups was statistically higher than that in the referent group. Error bars represent 95% confidence intervals for the prevalence ratios.

Figure. 

Prevalence ratios for all respondents in each concussion group (1, 2, or 3+ concussions) who reported a history of 0 lower extremity injuries as compared with the referent group (0 concussions, 0 lower extremity injuries). The prevalence of osteoarthritis in all concussion groups was statistically higher than that in the referent group. Error bars represent 95% confidence intervals for the prevalence ratios.

Close modal

The lifetime prevalence of OA among the ≤55 years group (33.9%) was smaller than that of the >55 years group (39.6%). In participants ≤55 years, the lifetime OA prevalence was higher in the 1 LE injury (26.4%; PR = 1.4; 95% CI = 1.0, 1.8) and 2+ LE injuries (43.4%; PR = 2.2; 95% CI = 1.8, 2.8; Table 2) groups compared with the 0 LE injuries group (19.5%). Lifetime OA prevalence in the >55 years group did not differ between the 1 LE injury and 0 LE injuries groups (34.3% versus 33.2%; PR = 1.0; 95% CI = 0.8, 1.3), yet the lifetime prevalence of OA in the 2+ LE injuries group was 40% higher than that of the 0 LE injuries group (PR = 1.4; 95% CI = 1.2, 1.6). Results were retained in the multivariate models.

In analyses using the 12-category exposure variable, the smaller lifetime prevalence of OA among participants ≤55 years was consistent among participants in each concussion/LE injury stratification. All univariate and multivariate PRs stratified by age are described in Table 4. Compared with the overall analyses, PRs for participants ≤55 years were larger, whereas PRs for participants >55 years, although statistically significant in some cases, were not as large as those in the ≤55 years group.

Table 4. 

Prevalence and Prevalence Ratios of Lifetime Prevalence of Osteoarthritis Within Each Group of Concussion and Lower Extremity Injury Counts Stratified by Age

Prevalence and Prevalence Ratios of Lifetime Prevalence of Osteoarthritis Within Each Group of Concussion and Lower Extremity Injury Counts Stratified by Age
Prevalence and Prevalence Ratios of Lifetime Prevalence of Osteoarthritis Within Each Group of Concussion and Lower Extremity Injury Counts Stratified by Age

Retired NFL players with a history of 3 or more concussions and 2 or more LE injuries reported the highest prevalence of OA. Concussion plus LE injury may be associated with OA. This effect is best seen in younger individuals (≤55 years) compared with older individuals (>55 years). Therefore, a concussion history in NFL players who also reported sustaining an LE joint injury may increase the risk of developing OA early in life (≤55 years). Our results also suggest a concussion dose-response relationship, as those who sustained multiple concussions demonstrated a higher prevalence of OA than those who received 0 or 1 concussion. To a lesser degree, we observed an LE injury dose-response relationship as well, with those who incurred 2 or more injuries reporting a higher prevalence of OA.

As seen in previous research,2022  we observed a dose-response relationship in which larger counts of LE injuries were associated with an increased lifetime prevalence of OA. Findings were similar within strata based on age. However, when also considering concussion history, we noted that the relative risk of OA associated with concussion existed even in the absence of self-reported LE injuries. Effect estimates were attenuated among the older age stratum (ie, >55 years). However, this was partially attributable to the attenuation of PRs due to the higher lifetime prevalence of OA in the referent group for the older age stratum (29.2%) compared with the younger age stratum (13.8%). Although these results highlight the limitations of PRs, which are bounded by a 0% to 100% range, they also suggest that concussion history, LE injury history, and age are associated with lifetime prevalence of OA.

Before considering possible explanations for the connection between concussion and OA, it is important to acknowledge the limitations of our work. Our outcomes were all survey based, and responses could be influenced by recall bias. A previous study15  of data from the same survey demonstrated moderate to good reliability in retired NFL players for self-reporting concussion (weighted Cohen k = 0.59) and LE injury history (weighted Cohen k ≥ 0.43). Unfortunately, the Health Survey of Retired NFL Players does not ask participants to specify which joints were affected by OA. Although OA commonly develops in joints of the upper extremity (eg, the hands), hand OA rarely develops in isolation, as most patients with hand OA also have symptomatic OA of the knee or lumbar spine.32  It is critical to acknowledge that all data were collected retrospectively and based on survey responses from retired NFL players only. We were unable to directly establish a causal association between concussion history and OA or to ascertain the exact time from injury (either concussion or LE injury) to the onset of OA. We also lacked data on concussions sustained before the participants' careers in the NFL, history of LE surgery, and BMI throughout their careers, all of which could influence OA progression. Previous authors1317  have linked concussion with LE injury but were unable to explore long-term outcomes. There is also evidence of a strong link between LE injury and OA.33  We sought to build on these publications by investigating the moderating effect of concussion on OA. Acknowledging the lack of causality in our report, we believe it is important to discuss several underlying constructs that may have contributed to the increased prevalence of OA in retired football players who experienced multiple concussions. Exploring these hypotheses further will help researchers and clinicians to develop intervention strategies targeting the underlying factors contributing to the increased prevalence of OA in retired NFL players who sustained concussions during their professional careers.

Aberrant gait biomechanics after concussion may influence OA development. Specifically, gait velocity was reduced immediately after concussion,3436  whereas frontal-37  and sagittal-plane center-of-mass range of motion increased.35  Motor-control strategy alterations appear postconcussion, as evidenced by altered peak propulsive and braking forces for up to 10 days after the injury.9  Traditional clinical measures indicate that postural control appears to return to normal within several days of injury,1,38  but other, more in-depth measures suggest that deficits persist beyond the athlete's return to play postconcussion.12,39  Together, these results imply that neuromuscular control is affected acutely and these changes may persist after the return to participation postconcussion. These findings are important, as aberrant gait biomechanics, which may be linked to changes in neuromuscular control, have been implicated in the progression of OA.18,19  Although this is still a hypothesis, an athlete who sustains multiple concussions and LE injuries at a relatively young age may alter his or her gait biomechanics. Our data suggest that concussion may be a more significant moderator of OA in those aged 55 and younger. Gait changes resulting from concussion may contribute to the increased prevalence of early-onset OA in retired NFL players. Linking potential biomechanical changes after concussion with aberrant gait biomechanics after LE injury may provide important information as clinicians and researchers seek effective interventions.

Appropriate motor control requires the efficient integration of multiple systems within a short period of time. Sensory and visual cues prompt a cognitive response. The primary motor cortex, in conjunction with several other brain regions, is responsible for planning and executing movement. Motor-evoked potentials (MEPs) provide useful information about the integrity of the motor cortex and descending motor pathways.40  When an external stimulus is applied to the motor cortex, surface electromyography can measure outcomes related to MEPs.4042  Several groups4346  have demonstrated decreased excitability of the primary motor cortex after concussion. Specifically, compared with healthy control participants, concussed participants displayed less intracortical facilitation,44  increased intracortical inhibition,43  increased MEP latency, and decreased MEP amplitude.45,46  Researchers14,15  have hypothesized that these cortical disruptions may increase the risk of musculoskeletal injury postconcussion. These disruptions may linger for years after the concussion,47  resulting in subtle yet important changes in functional movement. Although gross alterations in motor function are not common postconcussion, subtle persistent cortical-activation changes may alter movement biomechanics, increasing the risk of degenerative conditions such as OA. As this remains a hypothesis, future authors should prospectively investigate MEP alterations after concussion to determine a cortical recovery timeline.

Our findings cause concern for the long-term physical health of retired NFL players who have sustained multiple concussions and LE injuries. Despite our results, participation in sports provides numerous physical,48  psychological,49  and cognitive50  benefits. We believe our findings underscore the need to identify cortical impairments or other mechanisms that may lead to the increased prevalence of OA in retired football players who have sustained concussions. Our cohort of retired NFL players, as well as other current and former athletes, may benefit from long-term interventions aimed at correcting aberrant biomechanics resulting from a combination of LE injuries and concussions. We believe our results may help to further identify athletes who may be at increased risk of long-term degenerative conditions such as OA. Future investigators should seek to determine the direct cause of the increased risk of musculoskeletal injury after concussion, along with the associated mechanisms by which concussion appears to moderate OA prevalence in combination with a history of joint injury. If the underlying pathophysiology behind the increased risk can be identified, intervention strategies can be developed to mitigate the increased risk of injury and increased prevalence of OA after concussion and LE injury.

Our results suggest that concussion may be associated with OA in retired NFL players. Participants with a history of concussion (1, 2, or 3+ injuries) and no LE injuries reported a significantly higher prevalence of OA than the referent group. This association appears to be strongest among retired players ≤55 years old. The number of concussions sustained may also be important, as players with multiple concussions demonstrated a higher prevalence of OA than those with 0 or 1 concussion. More work is needed to identify the underlying cortical mechanisms that may contribute to OA progression after concussion.

The General Health Survey data collected by the Center for the Study of Retired Athletes were enabled by external (NFL Players Association) and internal (University of North Carolina at Chapel Hill) funding.

1
Guskiewicz
KM,
Ross
SE,
Marshall
SW.
Postural stability and neuropsychological deficits after concussion in collegiate athletes
.
J Athl Train
.
2001
;
36
(
3
):
263
273
.
2
Schatz
P,
Pardini
JE,
Lovell
MR,
Collins
MW,
Podell
K.
Sensitivity and specificity of the ImPACT Test Battery for concussion in athletes
.
Arch Clin Neuropsychol
.
2006
;
21
(
1
):
91
99
.
3
McCrea
M,
Guskiewicz
KM,
Marshall
SW,
et al.
Acute effects and recovery time following concussion in collegiate football players: the NCAA Concussion Study
.
JAMA
.
2003
;
290
(
19
):
2556
2563
.
4
McCrea
M,
Guskiewicz
K,
Randolph
C,
et al.
Effects of a symptom-free waiting period on clinical outcome and risk of reinjury after sport-related concussion
.
Neurosurgery
.
2009
;
65
(
5
):
876
882
.
5
Martini
DN,
Sabin
MJ,
DePesa
SA,
et al.
The chronic effects of concussion on gait
.
Arch Phys Med Rehabil
.
2011
;
92
(
4
):
585
589
.
6
Howell
DR,
Osternig
LR,
Chou
LS.
Adolescents demonstrate greater gait balance control deficits after concussion than young adults
.
Am J Sports Med
.
2015
;
43
(
3
):
625
632
.
7
Parker
TM,
Osternig
LR,
van Donkelaar
P,
Chou
LS.
Recovery of cognitive and dynamic motor function following concussion
.
Br J Sports Med
.
2007
;
41
(
12
):
868
873
.
8
Slobounov
SM,
Zhang
K,
Pennell
D,
Ray
W,
Johnson
B,
Sebastianelli
W.
Functional abnormalities in normally appearing athletes following mild traumatic brain injury: a functional MRI study
.
Exp Brain Res
.
2010
;
202
(
2
):
341
354
.
9
Buckley
TA,
Munkasy
BA,
Tapia-Lovler
TG,
Wikstrom
EA.
Altered gait termination strategies following a concussion
.
Gait Posture
.
2013
;
38
(
3
):
549
551
.
10
Howell
DR,
Osternig
LR,
Chou
LS.
Return to activity after concussion affects dual-task gait balance control recovery
.
Med Sci Sports Exerc
.
2015
;
47
(
4
):
673
680
.
11
Fait
P,
Swaine
B,
Cantin
JF,
Leblond
J,
McFadyen
BJ.
Altered integrated locomotor and cognitive function in elite athletes 30 days postconcussion: a preliminary study
.
J Head Trauma Rehabil
.
2013
;
28
(
4
):
293
301
.
12
Slobounov
S,
Cao
C,
Sebastianelli
W,
Slobounov
E,
Newell
K.
Residual deficits from concussion as revealed by virtual time-to-contact measures of postural stability
.
Clin Neurophysiol
.
2008
;
119
(
2
):
281
289
.
13
Nordstrom
A,
Nordstrom
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
(
19
):
1447
1450
.
14
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
(
12
):
2487
2492
.
15
Pietrosimone
B,
Golightly
YM,
Mihalik
JP,
Guskiewicz
KM.
Concussion frequency associates with musculoskeletal injury in retired NFL players
.
Med Sci Sports Exerc
.
2015
;
47
(
11
):
2366
2372
.
16
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
(
3
):
742
747
.
17
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
(
15
):
926
931
.
18
Palmieri-Smith
RM,
Thomas
AC.
A neuromuscular mechanism of posttraumatic osteoarthritis associated with ACL injury
.
Exerc Sport Sci Rev
.
2009
;
37
(
3
):
147
153
.
19
Zeni
JA
Jr,
Higginson
JS.
Gait parameters and stride-to-stride variability during familiarization to walking on a split-belt treadmill
.
Clin Biomech (Bristol, Avon)
.
2010
;
25
(
4
):
383
386
.
20
Cooper
C,
Snow
S,
McAlindon
TE,
et al.
Risk factors for the incidence and progression of radiographic knee osteoarthritis
.
Arthritis Rheum
.
2000
;
43
(
5
):
995
1000
.
21
Blagojevic
M,
Jinks
C,
Jeffery
A,
Jordan
KP.
Risk factors for onset of osteoarthritis of the knee in older adults: a systematic review and meta-analysis
.
Osteoarthritis Cartilage
.
2010
;
18
(
1
):
24
33
.
22
Muthuri
SG,
McWilliams
DF,
Doherty
M,
Zhang
W.
History of knee injuries and knee osteoarthritis: a meta-analysis of observational studies
.
Osteoarthritis Cartilage
.
2011
;
19
(
11
):
1286
1293
.
23
Chu
CR,
Andriacchi
TP.
Dance between biology, mechanics, and structure: a systems-based approach to developing osteoarthritis prevention strategies
.
J Orthop Res
.
2015
;
33
(
7
):
939
947
.
24
Howell
DR,
Osternig
LR,
Koester
MC,
Chou
LS.
The effect of cognitive task complexity on gait stability in adolescents following concussion
.
Exp Brain Res
.
2014
;
232
(
6
):
1773
1782
.
25
Chiu
SL,
Osternig
L,
Chou
LS.
Concussion induces gait inter-joint coordination variability under conditions of divided attention and obstacle crossing
.
Gait Posture
.
2013
;
38
(
4
):
717
722
.
26
Golightly
YM,
Marshall
SW,
Callahan
LF,
Guskiewicz
K.
Early-onset arthritis in retired National Football League players
.
J Phys Act Health
.
2009
;
6
(
5
):
638
643
.
27
Guskiewicz
KM,
Marshall
SW,
Bailes
J,
et al.
Association between recurrent concussion and late-life cognitive impairment in retired professional football players
.
Neurosurgery
.
2005
;
57
(
4
):
719
726
.
28
Greenland
S.
Model-based estimation of relative risks and other epidemiologic measures in studies of common outcomes and in case-control studies
.
Am J Epidemiol
.
2004
;
160
(
4
):
301
305
.
29
Zou
G.
A modified poisson regression approach to prospective studies with binary data
.
Am J Epidemiol
.
2004
;
159
(
7
):
702
706
.
30
Spiegelman
D,
Hertzmark
E.
Easy SAS calculations for risk or prevalence ratios and differences
.
Am J Epidemiol
.
2005
;
162
(
3
):
199
200
.
31
Losina
E,
Weinstein
AM,
Reichmann
WM,
et al.
Lifetime risk and age at diagnosis of symptomatic knee osteoarthritis in the US
.
Arthritis Care Res (Hoboken)
.
2013
;
65
(
5
):
703
711
.
32
Nelson
AE,
Renner
JB,
Schwartz
TA,
Kraus
VB,
Helmick
CG,
Jordan
JM.
Differences in multijoint radiographic osteoarthritis phenotypes among African Americans and Caucasians: the Johnston County Osteoarthritis Project
.
Arthritis Rheum
.
2011
;
63
(
12
):
3843
3852
.
33
Richmond
SA,
Fukuchi
RK,
Ezzat
A,
Schneider
K,
Schneider
G,
Emery
CA.
Are joint injury, sport activity, physical activity, obesity, or occupational activities predictors for osteoarthritis? A systematic review
.
J Orthop Sports Phys Ther
.
2013
;
43
(
8
):
B515
B519
.
34
Catena
RD,
van Donkelaar
P,
Chou
LS.
Altered balance control following concussion is better detected with an attention test during gait
.
Gait Posture
.
2007
;
25
(
3
):
406
411
.
35
Parker
TM,
Osternig
LR,
Van Donkelaar
P,
Chou
LS.
Gait stability following concussion
.
Med Sci Sports Exerc
.
2006
;
38
(
6
):
1032
1040
.
36
Catena
RD,
van Donkelaar
PV,
Chou
LS.
Cognitive task effects on gait stability following concussion
.
Exp Brain Res
.
2007
;
176
(
1
):
23
31
.
37
Parker
TM,
Osternig
LR,
Lee
HJ,
Donkelaar
P,
Chou
LS.
The effect of divided attention on gait stability following concussion
.
Clin Biomech (Bristol, Avon)
.
2005
;
20
(
4
):
389
395
.
38
Riemann
BL,
Guskiewicz
KM.
Effects of mild head injury on postural stability as measured through clinical balance testing
.
J Athl Train
.
2000
;
35
(
1
):
19
25
.
39
Cavanaugh
JT,
Guskiewicz
KM,
Giuliani
C,
Marshall
S,
Mercer
VS,
Stergiou
N.
Recovery of postural control after cerebral concussion: new insights using approximate entropy
.
J Athl Train
.
2006
;
41
(
3
):
305
313
.
40
Rossini
PM,
Barker
AT,
Berardelli
A,
et al.
Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee
.
Electroencephalogr Clin Neurophysiol
.
1994
;
91
(
2
):
79
92
.
41
Hallett
M.
Transcranial magnetic stimulation: a primer
.
Neuron
.
2007
;
55
(
2
):
187
199
.
42
Groppa
S,
Oliviero
A,
Eisen
A,
et al.
A practical guide to diagnostic transcranial magnetic stimulation: report of an IFCN committee
.
Clin Neurophysiol
.
2012
;
123
(
5
):
858
882
.
43
De Beaumont
L,
Mongeon
D,
Tremblay
S,
et al.
Persistent motor system abnormalities in formerly concussed athletes
.
J Athl Train
.
2011
;
46
(
3
):
234
240
.
44
Powers
KC,
Cinelli
ME,
Kalmar
JM.
Cortical hypoexcitability persists beyond the symptomatic phase of a concussion
.
Brain Inj
.
2014
;
28
(
4
):
465
471
.
45
Livingston
SC,
Goodkin
HP,
Hertel
JN,
Saliba
EN,
Barth
JT,
Ingersoll
CD.
Differential rates of recovery after acute sport-related concussion: electrophysiologic, symptomatic, and neurocognitive indices
.
J Clin Neurophysiol
.
2012
;
29
(
1
):
23
32
.
46
Livingston
SC,
Saliba
EN,
Goodkin
HP,
Barth
JT,
Hertel
JN,
Ingersoll
CD.
A preliminary investigation of motor evoked potential abnormalities following sport-related concussion
.
Brain Inj
.
2010
;
24
(
6
):
904
913
.
47
De Beaumont
L,
Theoret
H,
Mongeon
D,
et al.
Brain function decline in healthy retired athletes who sustained their last sports concussion in early adulthood
.
Brain
.
2009
;
132
(
pt 3
):
695
708
.
48
Drake
KM,
Beach
ML,
Longacre
MR,
et al.
Influence of sports, physical education, and active commuting to school on adolescent weight status
.
Pediatrics
.
2012
;
130
(
2
):
e296
e304
.
49
Eime
RM,
Young
JA,
Harvey
JT,
Charity
MJ,
Payne
WR.
A systematic review of the psychological and social benefits of participation in sport for adults: informing development of a conceptual model of health through sport
.
Int J Behav Nutr Phys Act
.
2013
;
10
:
135
.
50
Hillman
CH,
Erickson
KI,
Kramer
AF.
Be smart, exercise your heart: exercise effects on brain and cognition
.
Nat Rev Neurosci
.
2008
;
9
(
1
):
58
65
.