November 2017

BRAINS, SPRAINS, AND CHRONIC PAIN: Concussion consequences may include osteoarthritis

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As a growing number of studies report associa­tions between concussion and musculoskeletal injury risk, new research suggests concussed athletes may also have an increased risk of osteoarthritis later in life.

By Robert C. Lynall, PhD, ATC; Timothy C. Mauntel, PhD, ATC; David R. Howell, PhD, ATC; and Thomas A. Buckley, EdD, ATC

Concussion is a common injury in athletics, accounting for about 7% of college sports injuries1 and about 13% of high school sports injuries.2 Traditionally, a multifaceted approach to concussion diagnosis and management is recommended due to the injury’s individualized nature. The assessment battery, at a minimum, should consist of symptom, static balance, and neurocognitive assessments,3,4 and may often be employed at multiple times throughout an athlete’s concussion recovery. The same tests, or a similar set of tests, along with a thorough clinical examination, are typically used to determine when the athlete can return to physical activity. During the rehabilitation process, increasingly strenuous physical activity is introduced to the athlete in a stepwise progression before the athlete is allowed to return fully to sport participation.3,4

Numerous investigators have reported that static balance deficits exist acutely following concussion,5,6 making static balance assessment an important concussion assessment battery component. These deficits are commonly evaluated by clinicians in the field using a balance assessment such as the Balance Error Scoring System (BESS).6 This test has been validated against sophisticated force plate technology,7 and is preferred by clinicians due to its quick administration and inexpensive cost (a foam pad and stopwatch are all that is needed). Researchers have reported observable BESS deficits for several days after concussion,6,8 with most published data revealing a return to normal static balance (based on various balance assessments) within two to 10 days, often despite the presence of ongoing symptom or neurocognitive impairments.9-11

But are athletes truly recovered once they achieve baseline or normal levels on static balance assessments, or are the assessments not sensitive enough to detect lingering effects of the brain injury? Further, do static balance assessments truly reflect the dynamic demands of competitive sports?

Movement deficits after concussion

Recently, researchers have sought ways to investigate balance control during a movement, such as gait.12-15 This is a step in the right direction to better identify dynamic balance deficits following concussion, but athletes are often required to function in a highly dynamic sports environment in which they perform complicated motor responses specific to multiple cognitive stimuli. As an example, a football wide receiver runs a specific route cued from memory and must instantaneously react to several sources of visual and auditory cues, such as the position of the defenders around him or the trajectory of the ball thrown in his direction.

Although this type of complex motor-cognitive interaction is difficult to simulate in a research environment, investigators have designed tests pairing standard gait, and variations of standard gait such as stopping/starting and stepping over an obstacle, with cognitive tasks like counting backwards by sevens, answering simple questions (eg, what day is it?), and reacting to visual stimuli with a verbal response.12-14,16,17 This dual-task paradigm, while not directly simulating the sports environment, may better reflect the motor-cognitive interface required during sports than simply performing a motor or a cognitive task in isolation.

Using dual-task methodology, researchers have observed gait deficits that linger beyond those associated with traditional static balance assessments. Importantly, in many cases, deficits during dual-task paradigms often linger beyond the athlete’s return to play or after they report their symptoms have recovered.18-21

Some dual-task gait outcomes commonly reported include whole body center of mass movement,22 gait speed,23 and obstacle clearance height.21,24 Typically, concussed individuals demonstrate more conservative gait patterns compared with matched controls by slowing their average gait speed,23 taking shorter strides,25 and increasing obstacle clearance height.21 Concussed participants also display less stable walking patterns than controls, as evidenced by greater and faster center of mass sway.18,22,26 Similar findings have been observed in college-aged participants,23 adolescents,13,18,26 and children.20,25

Although gait after concussion has been extensively studied, less is known about potential movement deficits during more dynamic sport-like movements. One research group investigated lower extremity muscle stiffness in a group of concussed college football players (n = 13) and a group of uninjured players (n = 26) during a jump-landing task at pre- and postseason.27 There were no group differences at the pre- or postseason time points, but the concussed group dem­on­strated decreased knee and leg stiffness and increased hip stiffness from pre- to postseason, while no stiffness values changed from pre- to postseason in the control group.

Stiffer landings (less sagittal plane joint displacement) increase both ground reaction forces and loading rates, which increases injury risk.28,29 More erect landing postures increase landing forces and alter lower extremity muscle activation patterns.30 Altered muscular activation patterns inhibit the lower extremity musculature’s ability to attenuate landing forces, which results in greater anterior tibial shear forces, a primary predictor of anterior cruciate ligament injury.30

In another study, Lapointe et al31 investigated lower extremity kinematics during several cutting tasks in nine young adults with a concussion history and 10 controls. The authors reported that as task complexity increased (cognitive demands of the cutting task increased), concussed participants dem­onstrated significant center of mass displacement increases relative to controls. Several other kinematic differences were observed, such as less knee external rotation and less knee varus during cutting tasks in concussed participants than in control participants.

In both of the aforementioned studies, outcomes were measured after participants were deemed clinically recovered from concussion (mean time since concussion, 49.9 days for Dubose et al;27 3.1 years for Lapointe et al31), suggesting lingering dynamic movement deficits similar to those described in the gait literature.

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Musculoskeletal injury risk

One consequence of functional movement alterations following concussion may be an increased risk of musculoskeletal injury for athletes who have clinically recovered from concussion and returned to sport. This increased musculoskeletal injury risk has been reported across a number of studies with a variety of methodologies and study populations, including professional,32-34 college,35-39 and high school athletes.40 Increased musculoskeletal injury risk following concussion in athletes has been reported to range from 90 to 365 days. Importantly, it is not clear when this increased injury risk may subside, as only preliminary findings have extended the data collection period beyond one year postconcussion. Kardouni et al observed Army soldiers had a 39% greater risk of lower extremity injury over a two-year period following concussion than soldiers who had not sustained concussions.41

The increased musculoskeletal injury risk is likely a multifaceted issue, but the exact mechanisms have not been identified. One theory is that increased risk may be due to unresolved neuromuscular impairments.35,42 Subclinical changes in the motor cortex may alter muscle recruitment, which in turn affects neuromuscular function and results in abnormal movement patterns.27 Additionally, any changes in the premotor cortex may interfere or delay motor planning and preparation, which could result in delayed reactions to external stimuli. Delayed reaction times have been proposed as one possible cause of increased injury risk following concussion, as athletes may not be able to appropriately respond to dynamic situations on the field or court.42,43

Aberrant movement patterns, such as alterations in kinematics and kinetics, are a primary predictor of acute and chronic lower extremity injuries.44-50 Poor movement patterns can result from static skeletal malalignments,51 but more commonly result from neuromuscular control deficiencies.44,52 Irregular movements during activities increases forces acting on normally aligned lower extremity segments, and may cause normal forces to act on abnormally aligned segments. Both of these can occur simultaneously, which results in further abnormal musculoskeletal loading and increased injury risk.51

A primary predictor of various lower extremities injuries is frontal knee plane position during functional tasks. When the knee assumes a valgus or varus position during activity, the joint is less stable and more susceptible to injury.53 As previously noted, a small sample of concussed athletes demonstrated knee kinematics that have previously been associated with ACL injury.31 Much more work is needed to understand how biomechanics may be altered following concussion in a dynamic setting.

Uncharacteristic movement patterns following concussion may be further compounded by altered trunk and lower extremity stiffness during physical activity. Lower extremity stiffness, either too much or too little, has been linked to greater lower extremity injury risk.54 Previously concussed individuals may adopt a more rigid (ie, stiff) landing pattern in an attempt to increase joint stability. However, more rigid landings result in a greater reliance on ligamentous tissues for joint control, which increases injury risk to these structures.55 Concussion may alter lower extremity stiffness, as described by Dubose et al,27 but the potential direct impact of these changes on lower extremity injury risk is unclear.

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Impact on long-term joint health

Because all the studies referenced above related to concussion and musculoskeletal injury risk are limited, in that they investigate only dynamic movement deficits and the increased musculoskeletal injury risk for a finite period after concussion, the long-term consequences of concussion with regard to musculoskeletal health are not clear. To begin exploring potential long-term risks, we investigated self-reported osteoarthritis (OA) prevalence in retired professional football players (n = 2696).56

Uncharacteristic gait biomechanics57,58 and traumatic lower extremity injury59-61 have been associated with an increased risk of lower extremity OA, especially knee OA. Because gait changes have been described following concussion, and the timetable for their full recovery is not known,19,62 and because concussion increases the risk of musculoskeletal injury for an unknown time,32-40 we hypothesized that retired professional football players with a concussion history would have a higher OA prevalence than those with no concussion history.

After controlling for body mass index (BMI), age at the time of the survey, and total years playing professional football, we observed a significantly higher prevalence of OA (not specified by joint) in those with a concussion history than in those without a concussion history. Specifically, among players with a history of traumatic lower extremity injury (collateral knee ligament tear, ACL/posterior cruciate ligament tear, meniscal tear, hamstrings or quadriceps rupture, calf/Achilles rupture, ankle ligament rupture, ankle/foot fracture), we found those with one concussion had a 40% higher OA prevalence, and those with two or more concussions had a 70% higher OA prevalence, compared with those with no concussion history.

We were also interested in early onset OA in this cohort, and hypothesized that concussion-related gait changes may hasten OA onset. Thus, we compared OA prevalence in those younger than 55 years based on concussion and traumatic lower extremity injury history (as described above).

Retired players younger than 55 years with no history of traumatic lower extremity injury who had had two concussions had a 190% higher OA prevalence than similarly aged players with no concussion or lower extremity injury history. Similarly, those with no history of traumatic lower extremity injury and three or more concussions had a 110% higher OA prevalence than those with no concussion or lower extremity injury history. By comparison, OA prevalence in those older than 55 years with no history of traumatic lower extremity injury and two or more concussions did not differ significantly from the prevalence in those with no history of concussion or lower extremity injury.

Although it is important to consider methodological limitations to our work, such as the retrospective nature of the survey, non­specific OA diagnoses, and inability to directly link functional movement changes following concussion to OA development, these findings suggest the potential for long-term complications associated with concussion.

Clinical implications

Figure 1. Osteoarthritis prevalence ratios among retired professional football players with a history of traumatic lower extremity injury and/or concussion. All injury and concussion groupings had a significantly higher osteoarthritis prevalence compared to the 0 lower extremity injury/0 concussion history group except the 1 lower extremity injury/0 concussion history group and the 1 lower extremity injury/2 concussions history group.56

Concussion evaluation and management has evolved rapidly since the beginning of the 21st century. Dramatic increases in concussion knowledge have led to widespread changes in postconcussion assessment.3,4 But it is important to acknowledge there is much about the injury we still do not understand. Thus, we must continue looking for ways to enhance our clinical management of this brain injury, which is affecting a growing number of athletes worldwide. One aspect of concussion management evolution may involve incorporating standardized functional movement assessments in acute and return-to-play evaluations.

Static balance is commonly assessed as described above, but evaluating functional movement has proven more challenging, though new methods have allowed clinicians to test functional movement in a more feasible way.25,63-65 In both concussed and nonconcussed individuals, the addition of a dual task appears to affect movement and dynamic balance.12,26,66

Tandem gait has been suggested as a means of identifying dynamic balance deficits after concussion,67 though little research supports this suggestion.12 Clinically, tandem gait can be easily assessed by timing an athlete as she or he walks heel to toe along a piece of tape laid on the ground.

Preliminary research suggests adolescents and young adults with a concussion take significantly longer to complete dual-task tandem gait throughout the first two weeks following injury relative to uninjured controls.12 Additionally, children who were considered clinically recovered from concussion walked significantly more slowly during tandem gait than did matched controls.20 These results suggest the addition of tandem gait to a concussion assessment battery may have some clinical value, but much more research is needed before such a recommendation can be made.

Conclusions

A growing body of literature suggests musculoskeletal injury risk is increased following concussion,32-40 even after clinical recovery using recommended assessment tools. Furthermore, additional evidence suggests there is prolonged physiologic recovery after concussion,68 highlighting the need to continually evaluate and evolve the concussion assessment battery.

The study of functional movement and gait after concussion, especially when including cognitive dual tasks, will provide further insight into complete concussion recovery. A better understanding of the recovery time course for functional movement outcomes may lead to safer return-to-play policies, and the development of rehab­ilitation paradigms to reduce the short- and long-term consequences of movement deficiencies after concussion.

Robert C. Lynall, PhD, ATC, is an assistant professor in the UGA Concussion Research Laboratory, Department of Kinesiology, at the University of Georgia in Athens. Timothy C. Mauntel, PhD, ATC, is research director for the Military Orthopaedics Tracking Injuries and Outcomes Network (MOTION) in the Department of Orthopaedics at Walter Reed National Military Medical Center, and assistant professor in the Department of Surgery at the Uniformed Services University of the Health Sciences, both in Bethesda, MD. David R. Howell, PhD, ATC, is an assistant professor in the Department of Orthopedics at the University of Colorado School of Medicine and lead researcher for the Sports Medicine Center at Children’s Hospital Colorado, both in Aurora. Thomas A. Buckley, EdD, ATC, is an associate professor in the Department of Kinesiology and Applied Physiology at the University of Delaware in Newark.

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