May 2013

Concussion assessment: Neuromuscular concerns

5balance-shutterstock_45284800aBalance testing is already recommended for concussion assessment in athletes, but research suggests the connections between concussion and neuromuscular variables are even more complex, and the opportunities for intervention more numerous.

By Brent Harper, PT, DPT, DSc, OCS, FAAOMPT

The consensus statement1 emerging from the fourth International Consensus Conference on Concussion in Sport reported that various postural stability tests, ranging from the high-tech NeuroCom system, which uses force plates, to more clinical balance assessments, such as the Balance Error Scoring System (BESS), are valid and reliable tools for evaluating postconcussive athletes.

The statement’s authors, who convened in Zurich in December 2012 to advance the ongoing consensus-based approach to treatment of injured athletes, noted “postural stability testing provides a useful tool for objectively assessing the motor domain of neurological functioning, and should be considered as a reliable and valid addition to the assessment of athletes suffering from concussion, particularly where the symptoms or signs indicate a balance component.”1

Clinicians involved in the care of injured athletes—professional, elite, or recreational—should consider implementing postural control assessments to help identify those at risk for suffering a concussion (preconcussive screening) and in the management of postconcussion syndrome.

Concussion basics

Concussion falls within the broader diagnosis of mild traumatic brain injury (MTBI).2 Concussions in sports participants have been estimated at between 1.6 million and 3.8 million episodes annually, making it a significant issue for the general population and public health.2 More than 1.25 million high school athletes participate in sporting events annually, and more than 60,000 suffer concussions every year in the US, making this issue a public health concern for adolescents, as well.3 A number of concussions—between 15% and 45%—occur following a direct blow to the head during American football.4 Unfortunately, more than half of these athletes, at least 53%, did not report their concussion symptoms.4

Functional Movement Screen (FMS): A dynamic low-tech screen used to identify those who may be at risk for a musculoskeletal injury and to measure balance to quantify postural stability and control.

Functional Movement Screen (FMS): A dynamic low-tech screen used to identify those who may be at risk for a musculoskeletal injury and to measure balance to quantify postural stability and control.

The incidence of concussion in published reports varies, in part because older estimates included only those concussions associated with loss of consciousness. Underreporting, resulting from a lack of definitive diagnostic tools for identifying concussion symptoms without loss of consciousness and from a lack of standard concussion surveillance guidelines, may have  further confounded these older estimates. As more individuals become involved with sports and as community awareness of concussion grows, it is likely the published incidence will rise as concussions are more readily identified.5

Sport-related concussion can be a serious injury,4 especially for younger athletes, whose brains are still developing physically and cognitively,5 and is a highly debated topic in sports medicine.4,5 In Virginia, legislation became effective July 1, 2011, requiring local schools to develop concussion guidelines for identification and management of student-athletes who may have suffered a concussion. Components of the law include: (1) the parent or guardian and student-athlete must sign an annual statement after reviewing concussion educational material; (2) the student-athlete suspected of sustaining a concussion will be immediately removed from the activity; and (3) he or she will not be allowed to return to play that same day and will be allowed to return to sports only after being evaluated and cleared in writing by a licensed healthcare provider.6

Symptoms and physiology

Concussion is a closed-head brain injury resulting from direct impact to the head or from forces impacting the body causing force transmission to the head, similar to whiplash. Loss of consciousness is not required for diagnosis, though it sometimes occurs, and typically there are no physical changes visible on standard neuroimaging studies.

Assessment typically focuses on neurological domains, from subjective behavioral reports to objective physical signs such as impaired balance, sleep, and cognition. Student-athletes suspected of suffering a concussion display one or more of the following self-limiting symptoms: Headache, feeling “like in a fog,” emotional instability, loss of consciousness, amnesia, elevated behavioral irritability, sluggish mentation, delayed physical reaction time, drowsiness, or changes in normal sleep pattern.7

Similar to the forces in whiplash, shearing of the neurovascular elements occurs during a concussion due to the abrupt forces of acceleration and deceleration. This causes immediate depolarization of the nerves within the brain, which disrupts neuronal communication.8 In animal models, this neuronal disruption resulted in changes in the hippocampus and injury along the axons, impairing the blood-brain barrier homeostasis and resulting in neuronal death.9,10 Secondary to this neuronal membrane imbalance, potassium rushes into the extracellular space, causing a release of the excitatory amino acid glutamate, which potentiates potassium influx. The end result is additional depolarization and impairment of the nervous system. As the body attempts to restore homeostasis, it uses adenosine triphosphate and glucose to power sodium-potassium pumps. The blood-brain barrier impairment results in less blood flow to the brain and accumulation of lactate.5 Regulation of glucose, mitochondrial function, and blood flow is affected, resulting in a period of hyperglycolysis and followed by an induced cascade of neurochemical, ionic, and metabolic changes that alter cerebral glucose metabolism and blood flow, leading to metabolic famine.11,12 This brief period of neuronal starvation disrupts cognitive and motor function.

Because this pathophysiologic hypothesis has been observed only in animal models, it’s not yet clear how directly it can be applied to sports-related concussions in humans.5 However, the cognitive and motor impairments that are symptomatic of concussions suggest that such brain injuries can alter regulation of the cardiopulmonary system by the autonomic nervous system (ANS), as evidenced by exacerbation of concussive symptoms with heightened physical activity.2

Basic management components

Concussion management is challenging for any athlete, especially for those in collision sports, since players must adhere to mandated physical and cognitive rest until symptoms resolve; activities requiring concentration and attention (school work, reading, watching television, playing video games) worsen symptoms and delay recovery.7

A graded program of gradually increased physical exertion follows the mandatory rest until the player receives medical clearance to return to sports. The process may take days to weeks, exacerbating the anxiety an athlete, parent, or coach may feel about acknowledging concussion symptoms in the absence of an obvious sign, such as loss of consciousness or vomiting. While on cognitive rest, a student-athlete will fall behind in classes and academic performance may suffer.4 Thus, cognitive assessment tools are essential components to the recovery process, ensuring that the athlete resumes academic activities as the brain regains its baseline cognitive abilities. Concussion management should remain a gradual, stepwise, and closely monitored program4 in which resolution of all symptoms is confirmed with objective postural stability and neurocognitive tests compared with preseason baseline measures.

Protective equipment

American football organizations have instituted many changes to decrease the incidences of direct head collisions and of concussion; however, due to the nature of the sport, these risks cannot be eliminated completely. The primary concussion-related protective equipment includes the helmet and, to a lesser extent, the mouth guard.13

Rowson and Duma14 used accelerometers and developed the Virginia Tech STAR (summation of tests for the analysis of risk) helmet rating evaluation system to measure impact forces on helmets in an effort to rate multiple brands of adult helmets by degree of protection from concussive forces. The National Operating Committee on Standards for Athletic Equipment15 criticized this appraisal because results used to predict concussive probability were derived using data from a single linear acceleration impact, whereas concussive events are multifactorial—involving force changes, linear and rotational accelerations, prior concussive history, general health, helmet fit, and, possibly, genetics. Furthermore, it takes more than helmets to protect a player from a concussive event. Daneshvar et al16 agreed that the helmet rating study was limited because it studied only linear accelerations and did not account for rotation acceleration.

Rowson and Duma13 suggest that healthcare professionals could use data from accelerometers in players’ helmets to monitor the impact forces to the head; forces exceeding an accepted standard value would initiate a concussion examination regardless of whether the player reported the incident or complained of symptoms. Measuring the forces and subsequently removing the athlete for examination could dramatically reduce the risk of an undiagnosed and untreated concussive event, as well as reducing the risk of second impact syndrome. The researchers also compared linear and rotational acceleration and, in answer to the criticisms of the STAR helmet rating system, proposed that either force could be used independently to rate helmets for product safety in a laboratory setting. Although helmets are not the only factor in limiting concussive events, research will undoubtedly continue to assess the role they play in concussion incidence reduction.

Neuromuscular and cognitive testing

The concussion rehabilitation team includes physicians, athletic trainers, neuropsychologists, and physical therapists. Two primary factors used to evaluate functional recovery after a concussion are postural balance testing, which may be done using computerized perturbation devices, and cognitive assessment, such as the computer-administered neuropsychological test battery called the Immediate Postconcussion and Cognitive Test (ImPACT).3,17 Maintaining postural stability involves complex coordination and integration of multiple sensory, motor, and biomechanical components. Following a concussion, the visual, vestibular, and somatosensory systems fail to function optimally; therefore, assessment should include postural stability and cognitive processing.17

NeuroCom system: Computerized perturbation with force plate technology to measure balance to quantify postural stability and control.

NeuroCom system: Computerized perturbation with force plate technology to measure balance to quantify postural stability and control.

Research has shown that the neuropsychological ImPACT test is a reliable18 and valid19 concussion assessment tool that is both sensitive and specific when used in younger athletes.20 The incidence and likelihood of concussion based on preinjury postural stability and cognitive function, however, is unknown.

Balance testing is a method of assessing postural control and stability. According to Smith, Ulmer, and Wong:21 “Postural control is the ability to control the position of the body’s center of mass (COM) over its base of support (BOS) to prevent the body from falling … The process by which humans maintain the integrity of their postural control is referred to as balancing. Stability exists when the vertical line of gravity from the COM falls within the BOS, and stability improves with a larger BOS, a lower COM, and/or a more central COM within the same BOS. Postural control is a complex process requiring integration of sensory information (somatosensory, visual, and vestibular feedback) and execution of appropriate postural responses.”

Muir et al22 link balance with cognitive function, as well as musculoskeletal efficiency, writing: “Postural stability is a complex process that involves the rapid, automatic integration of information from the vestibular, somatosensory, visual, and musculoskeletal systems in the presence of cognition, which includes attention and reaction time. The measurement tools used to evaluate balance in the clinical setting are a means of quantifying the working capacity of the sum of the components that enable postural stability.”

Balance testing devices and other clinical balance evaluations (such as the BESS) can be used to measure postural stability objectively. Measurable balance deficits have been recorded up to 72 hours postconcussion.7 Postural stability testing provides a useful tool for objectively assessing the motor domain of neurological functioning and should be considered a reliable and valid option for postconcussion assessment, particularly when symptoms or signs indicate the injury has affected balance.7,17,23

Neuropsychological testing, such as ImPACT, is an essential—and, according to some, the most critical4—component of concussion assessment.6 Resolution of cognitive dysfunction usually occurs after other symptoms have resolved. Therefore, student-athletes may seem to have complete resolution of typical concussion symptoms without complete cognitive recovery, leaving them especially vulnerable to additional brain injury. Thus, neuropsychological testing is an extremely useful evaluation tool in return-to-play decisions.7,23

Covassin et al23 conducted a cohort study examining and comparing the neurocognitive performance (using ImPACT) and postural stability (measured with the BESS) of high school and collegiate athletes who had suffered a concussion. According to their data, female athletes suffered more impairments and symptoms than their statistically equivalent male athlete counterparts.

Guskiewicz et al17 assessed baseline postural stability (assessed with the NeuroCom system and the BESS) and cognitive function (five distinct neuropsychological tests excluding the ImPACT assessment) in collegiate athletes to examine the progression of symptoms following a concussion, particularly among those whose concussive event involved a loss of consciousness. Concussion was associated with significant postural stability impairments compared to baseline, but baseline postural stability scores did not differ significantly between those who went on to sustain a concussion and those who did not. Riemann et al24 confirmed the value of the BESS as an important clinical return-to-play decision-making tool for clinicians when high-tech diagnostic equipment is not available.

Mulligan et al25 assessed neurocognitive (ImPACT) and postural balance (BESS) scores of asymptomatic nonconcussed collegiate football players 48 hours after the last game of an 11-game season and compared results with preseason baseline scores. Although these individuals were not diagnosed with concussion throughout the season because they did not present with one or more standard signs and symptoms of concussion, they demonstrated deficits in cognitive and balance function as tested by ImPACT and BESS.25 The scores suggested that 71% of those tested had at least one deficit related to neurocognitive impairments, postural instability, or both. Of those, 32% exhibited statistically significant balance impairment. Extrapolating from their data, the authors noted that athletes may not recognize the signs of a concussion and, therefore, fail to seek out a healthcare professional for an examination.

The presence of cognitive and balance deficits may be considered potential symptoms of concussion, and, therefore, important components that clinicians should consider integrating into concussion education for both athletes and the practitioners managing their health.

Talavage et al26 found that high school football players who experienced head collision events yet remained free from typical concussive signs and symptoms had neurocognitive (ImPACT) and neurophysiological (functional magnetic resonance imaging) changes comparable to or exceeding those of players who had been medically diagnosed with concussion. These findings are consistent with the previous study by Mulligan et al25 and emphasize the pressing need for more accurate diagnostic criteria and related assessments to predict those at elevated risk for concussion and to identify those who may be affected by concussion despite appearing asymptomatic by current diagnostic standards. As concussions continue to go unrecognized and players fail to undergo clinical evaluation, continuing to participate in high-risk play, student-athletes will be at greater risk of progressive neurological injury and mounting cognitive deficits.26

Concussion and musculoskeletal injury

When pain is present, normal movement strategies and patterns are altered. Unfortunately, changes in motor control and adaptation occurring secondary to pain are neither uniform nor predictable.27

Swanik et al28 found a predictive relationship between ImPACT assessment scores and the relative risk of noncontact anterior cruciate ligament (ACL) injuries. According to their data, individuals who went on to suffer noncontact ACL injuries had lower baseline ImPACT scores than their uninjured counterparts. The authors postulated that complex movements require more neurons processing information more rapidly than with less-complex activity. A decrease in neurocognitive processing may alter physical reaction time and motor coordination, and these cognitive strains would be worsened further in a poorly conditioned or fatigued athlete. These neuromuscular control disruptions alter dynamic control during complex movements, increasing the risk of injury.

Hutchison et al29 compared cognitive function among athletes with concussion, those with musculoskeletal injuries, and those without injury to determine if cognitive impairment was exclusive to head impact trauma or if other injuries could have a similar result. The researchers wondered if indirect injury-related mechanisms, such as pain, could affect cognitive function as measured by the Automated Neuropsychological Assessment Metrics (ANAM). According to their data, those with musculoskeletal injuries performed more poorly on some aspects of the ANAM than healthy controls. This suggests that cognitive function can be impacted negatively by injuries other than a concussive event, indicating that other injury factors influence cognitive function as measured by neuropsychological assessment. This research substantiates the conclusions drawn by Swanik et al.28 Because of the low statistical power in the study by Hutchison et al,29 the authors were unable to draw strong conclusions as to why the athletes with musculoskeletal injuries had lower cognitive scores.

Hutchison et al’s findings were immediately challenged by Coldren et al,30 who expressed a concern that the data from the previous study would be misused; practitioners might attribute an athlete’s poor cognitive scores to a musculoskeletal injury and ignore the potential for concussion, especially when making return-to-play decisions. Hutchison et al’s response30 stated that concussion researchers should be aware that not every postinjury cognitive deficit can be attributed directly to brain injury, since other musculoskeletal injuries also can be associated with neuropsychological deficiencies.

It seems clear that there is a link between neuromuscular control and risk of musculoskeletal injury, as previously identified by the Functional Movement Screen (FMS).31,32 The FMS was found to have good intra-rater and inter-rater reliability.33 There also appears to be a link between those who suffer an injury and how they score on neuropsychological assessment tests.28,29 Currently, one can only speculate as to whether various balance tests, functional movement tests, and neurocognitive function tests could be useful to predict risk of concussion.

Concussive events appear to be multifactorial; risk factors include more than direct head impact alone, and protection probably involves more than choosing the correct protective equipment. Other risk factors might involve fatigue, pain, or previous injuries, which, in turn, affect body position, reaction time, functional movement patterns, and nervous system motor control patterns. In individuals without pain, neuromuscular motor control patterns can be screened objectively using a variety of functional tests, such as the FMS. Those with pain can be assessed methodically, using various clinical methods,34-38 and/or dynamically, using the selective functional movement assessment (SFMA),39 to determine potential for altered motor control.

Cognitive functional impairments have been identified both in individuals with musculoskeletal injuries and in those with concussions.28,29 Unfortunately, there are few studies directly correlating baseline neuropsychological measures, postural balance tests, and dynamic movement assessments—potential predictive tools for identifying those at risk for a concussion—with postplay concussion injury status. Such studies might be useful, not only to predict those at higher risk for concussion, but also to establish new diagnostic parameters for concussion based on comparison between baseline and postinjury assessments of neuropsychological, postural balance, and dynamic movement.

Future directions

In conjunction with return-to-play, current research should become more focused on concussion prevention. This may involve investigating the extent to which previous injuries and pain lead to impaired movement patterns that may make an injured athlete more susceptible to concussion. Just as the FMS31-33 has been demonstrated to be a reliable screening tool for musculoskeletal injury, there may be a link between optimal nonpainful neuromuscular control patterns and reduced incidence of some concussions, such as those resulting from indirect head trauma. Indirect concussion may involve a summation of events that gradually load the musculoskeletal tissues, priming the nervous system responses and eventually resulting in soft tissue changes similar to whiplash-associated disorders. These soft tissue changes occur in the muscles, ligaments, and other connective tissues. They may be expressed in multiple presentations, including tenderness, decreased muscle length, decreased cervical range of motion, decreased muscle function, dizziness, and decreased balance.40,41

The literature has not evaluated incidence of concussion in those with prior musculoskeletal injury. By establishing baseline levels and risk thresholds for neuromuscular test scores, it may be possible to reduce the risk of both musculoskeletal injury and indirect concussions. For example, requiring a minimum baseline score to participate in a sport associated with high risk of concussion (e.g., football) could discourage athletes from purposely underperforming on baseline tests to make any subsequent postconcussion deficits appear less severe. Neuromuscular control and movement pattern deficiencies could be addressed before the athlete was allowed into a competitive environment. Future preventive research could be directed at identifying a link between prescreened balance and cognitive scores and concussion risk and, if such a link exists, using a neuromuscular movement screen to identify at-risk athletes.

Brent Harper, PT, DPT, DSc, OCS, FAAOMPT, is an assistant professor in the Department of Physical Therapy at Radford University in Radford, VA.

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One Response to Concussion assessment: Neuromuscular concerns

  1. Lester Mayers MD says:

    The author of this article states that “research has shown that the neuropsychological ImPACT test is a reliable (18) and valid (19) concussion assessment tool that is both sensitive and specific when used in younger athletes (20)”. Readers of LER should know that these studies were performed and published by the owners and sellers of ImPACT in reputable journals without acknowledging their conflicts of interest. More recent studies have refuted the the reliability and validity of ImPACT and questioned its sensitivity, specificity and usefulness for the management of concussion.

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