Clinical Assessment of Balance in Adults with Concussion
ABSTRACT
Balance is a key component to the assessment of concussion injury; however, the efficacies of clinical tests used are currently under debate. It is questionable whether currently accepted methods of standing balance assessment quantify balance disturbances sufficiently to support decisions on recovery and return to play. Recent evidence of balance abnormalities postconcussion that linger beyond the typical 3to 5-day recovery period support arguments that currently available standing balance tests are not sensitive enough to determine recovery of function. This article discusses the current clinical tests used in the assessment of concussion in adults and their limitations and the evidence supporting continued balance dysfunction. Implications for the future of balance assessment in concussed adults and recommendations to clinicians for best practices are presented. KEYWORDS: Balance assessment, standing balance, vestibular,
sensory integration, concussion
Learning Outcomes: As a result of this activity, the reader will be able to (1) discuss the underlying mechanisms of balance control and the effects of concussion on these mechanisms; (2) summarize the current methods for balance assessment and their limitations; (3) discuss the implications of current evidence supporting lingering balance issues postconcussion; (4) apply the current state of knowledge of balance postconcussion to best practices when assessing concussion in adults.
1
Department of Applied Human Sciences, Faculty of Science, University Prince Edward Island, Charlottetown, Prince Edward Island, Canada; 2Interdisciplinary Health Sciences Ph.D. Program, University of Texas at El Paso, El Paso, Texas; 3Department of Physical Therapy, Campbell University, Buies Creek, North Carolina. Address for correspondence: Rebecca J. Reed-Jones, Ph.D., Department of Applied Human Sciences, Faculty of Science, University Prince Edward Island, 550 University
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Avenue, Charlottetown, PE, Canada, C1A 4P3 (e-mail: [email protected]). Concussion 101 for SLPs; Guest Editor, Anthony P. Salvatore, Ph.D., CCC-SLP Semin Speech Lang 2014;35:186–195. Copyright # 2014 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA. Tel: +1(212) 5844662. DOI: http://dx.doi.org/10.1055/s-0034-1384680. ISSN 0734-0478.
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Rebecca J. Reed-Jones, Ph.D.,1 Nicholas G. Murray, Ph.D.,2 and Douglas W. Powell, Ph.D.3
WHY BALANCE IS AN IMPORTANT COMPONENT OF CLINICAL ASSESSMENT OF CONCUSSION Balance is a dynamic action requiring control of the effects of gravity on the body. In bipedal quiet stance, humans are never motionless; small excursions or an observed sway occur and are a reflection of fine adjustments made by the muscles about the joints to continue alignment with gravitational forces.1 The motor control system receives information regarding the required magnitude and location of adjustments through the sensation and perception of orientation, position, and motion of the body and its segments by the sensory systems.2 As such, even the simple task of standing with 2 feet in upright stance requires integration of sensation, perception, and motor coordination. Any disruption within these processes can result in muscular maladjustments and result in inconsistent sway patterns. These abnormal sway patterns are the focus of balance assessment following a concussion.
WHAT OCCURS TO BALANCE CONTROL POSTCONCUSSION Balance disturbances occur in up to 80% of sport-related concussion injuries, with dizziness occurring in 75.6% of injuries.3,4 The most commonly measured balance variable is the presence or absence of increased sway and/or the magnitude of sway movement. The presence of increased sway is interpreted as a decrease in balance control. Measuring sway postconcussion using a quiet upright bipedal stance or static method suggests that a dysfunction of balance is greatest at 1 day postconcussion. Furthermore, the literature suggests that this dysfunction resolves within 3 to 5 days postconcussion. The recovery of balance also apparently precedes the recovery of cognitive performance and a decrease in postconcussion symptoms.5–10 However, there is increasing evidence to suggest that balance dysfunction can persist for weeks, months, and even years following a concussion.3,11–15 Although these data are based upon the use of static measures of balance, abnormal postural control has been demonstrated up to 30 days postinjury using dynamic balance and gait tasks.13,14 For a
summary of studies examining the resolution of balance dysfunction postconcussion, see Table 1. An important consideration regarding the differences in postural control recovery between static standing balance tests and dynamic balance/gait tests is that the traditional reliance upon static standing balance tests alone may result in a premature return-to-play decision. Such a premature decision may place an individual at greater risk for falling and/or collisions during play, as well as during activities of daily living. Therefore, susceptibility to a second concussion event is increased across all activities.
HYPOTHESIZED UNDERLYING MECHANISMS THAT ARE DISRUPTED DUE TO CONCUSSION Sensory information received from the visual system, the somatosensory system, and the vestibular system all contribute to the control of balance. Of the three sensory systems, the vestibular system may be a primary contributor to balance disruptions following concussion.6,8,12,16,17 The vulnerability of the vestibular system to damage following a concussion is certainly plausible; impacts in the cranial area can disturb the sensitive hair cells and interfere with sensation. However, the potential for physical damage sustained by the vestibular system from concussion injuries is still largely unknown. Another explanation regarding disruption of vestibular information suggests that axonal injury and edema caused by the impact interrupts vestibular afferents to the brain.18 Acute disruptions to afferent signals could explain the high incidence of dizziness and the loss of balance control within the first 24 hours following injury. Resolution of edema following injury could also explain gross recovery of balance within 72 hours postinjury. However, persistent balance issues indicate the potential for mechanisms beyond disruption due to edema. Recent studies support the hypothesis that a dysfunction in the control mechanisms of posture occurs at the sensory integration level.19,20 The central nervous system (CNS) may filter or reweight vestibular information during the acute recovery phase based on erroneous or
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BALANCE IN ADULTS WITH CONCUSSION/REED-JONES ET AL
during CTSIB BESS and SOT BESS BESS ApEn algorithm to COP
and high school)
16 athletes age 19.2 2.3 y 94 collegiate football players
570 football players
(collegiate and high school) 29 collegiate athletes
8 collegiate athletes
38 collegiate athletes
15 collegiate athletes
Riemann et al (2000)9 McCrea at el (2003)5
McCrea et al (2012)10
Cavanaugh et al (2006)16
Slobounov et al (2006)13
Slobounov et al (2008)14
Parker et al (2006)15 Up to 28 d
No, symptoms resolved earlier
No, symptoms resolved earlier
NA
No, symptoms resolved earlier
No, balance resolved earlier
Yes Yes
NA
Relation to Symptom Resolution
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Note: Top four studies used standard balance tests. Bottom four studies used novel approaches to balance assessment. Abbreviations: ApEn, approximate entropy; BESS, Balance Error Scoring System; COP, center of pressure; CTSIB, Clinical Test of Sensory Interaction and Balance; NA, not available; SOT, Sensory Organization Test.
dual-task level walking
Up to 30 d
COP from dynamic bal-
Up to 30 d
Up to 96 h
Up to 3 h postinjury
Up to 3 d Resolve 3–5 d
Up to 3–5 d
Significant Effects Present Postinjury
ance task Kinematics during single/
COP of standing balance during visual field motion
from SOT
Sway magnitude of COP
10 football players (collegiate
Guskiewicz et al (1996)6
Test
Population with Concussion
Summary of Studies Examining Recovery of Balance Postconcussion
Study
Table 1
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noisy sensory information derived from a damaged organ or disrupted afferent function due to edema.19–21 On resolution of vestibular information, the CNS must correctly reintegrate incoming vestibular sensory information with visual and somatosensory information. How and when the CNS does this following a concussion injury is still largely unknown and, therefore, could be a potential mechanism for continued balance dysfunction. However, without the use of brain imaging or direct measurements of the brain, this observation is speculative. To date, no literature has examined or observed direct damage to either the vestibular organs or vestibular nuclei. Until direct measurements occur, indirect measurements must suffice to rule out the contributions of the vestibular system to balance dysfunction after a concussion episode.
CURRENT TESTS USED TO ASSESS CONCUSSION The most commonly used tests to assess balance postconcussion are the Sensory Organization Test (SOT),22 the Clinical Test of Sensory Integration and Balance,23 the Romberg test,24,25 and the Balance Error Scoring System.9,26 These tests assess static standing balance control under varying sensory conditions. For a more exhaustive comparison of these tests in the assessment of concussion, see Guskiewicz.8 The SOT and Clinical Test of Sensory Interaction and Balance (CTSIB) were developed to assess contributions of the sensory systems to postural control. They are presented together because their procedures and interpretations are similar with CTSIB being a simpler and more inexpensive version of the SOT. The SOT was developed as a tool to examine the contributions of each sensory system to postural control as well as the adaptability of the CNS to select and use the most relevant sensory information.22 Therefore, the SOT not only provides insight into each system’s use but also provides insight into the effectiveness of the CNS to interpret and respond to erroneous information. The SOT apparatus consists of two moveable instrumented platforms that rotate and translate independently. The first platform contains the
support surface on which the patient stands. The second platform is composed of a visual surface that rotates about an axis that is colinear with the patient’s ankles and produces visual perturbations to the patient’s visual reference frame.22 Postural control assessment using the SOT is composed of an objective measurement of center of pressure (COP) path by a force platform. A force platform is an instrumented plate that records forces produced by an individual standing on the plate. COP is a measure derived from these forces and, as the name infers, is the center (or concentration) of these forces. The pattern of movement of the COP is a direct result of movements of the body on the plate. As such, it is an objective measure of balance. Measures of sway of the body’s center of mass can also be measured using a potentiometer attached at the hips. Since the development of this protocol, the apparatus of the SOT has been developed in a commercially available product, NeuroCom’s EquiTest (NeuroCom1 a division of Natus, Clackamas, OR). To address the issue of the practicality and expense of the apparatus in clinical settings Shumway-Cook and Horak developed the CTSIB.23 The CTSIB also has six conditions (three visual conditions and three surface conditions) for assessing a patient’s postural control (Fig. 1). The difference from the SOT is that the CTSIB uses foam under the feet to manipulate somatosensory information and a paper lantern placed over the head to manipulate visual references. These modifications allow the CTSIB to be less expensive. Assessment is composed of three measures: (1) the amount of time a patient can maintain stance, (2) a subjective assessment ranking the magnitude of sway observed in each condition, and (3) objective measurement of the body’s displacement via a plum line attached to the body. Studies have also used a force plate to objectively measure COP during these conditions.6 The benefit of both the SOT and CTSIB are that the results provide insight into which sensory system a patient relies on for postural control. The Romberg test is perhaps the oldest and most commonly used clinical test of postural control. The test itself is simple and requires a patient to stand first with the eyes open and then with the eyes closed. Standing can be done
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Figure 1 Comparison of sensory conditions of the Sensory Organization Test (SOT), Clinical Test of Sensory Integration and Balance (CTSIB), and Balance Error Scoring System (BESS). Note that the sensory manipulations in the SOT and CTSIB are identical, despite the different methods to produce the manipulations. The BESS is a simplification, including only conditions 2 and 5 of the SOT and CTSIB. The major difference is that the BESS has three stance configurations for each sensory condition, two feet, single foot, and heel-totoe stance (not represented in the figure).
in several different configurations; the most common configuration is feet together; however, tandem stance (heel to toe) can also be used and is a more challenging test.25 Typically, the Romberg test is a positive or negative rating, with a positive rating given when increased sway (e.g., magnitude and/or velocity) is observed when the eyes are closed.27 The Romberg test provides insight into whether somatosensory and vestibular sensory information are providing sufficient information to maintain stance. When a positive sign is present, at least one of the remaining sensory systems is contributing to inappropriate postural adjustments. However, the test is limited in any further interpretation to what is occurring within those two sensory systems. A positive Romberg could be the result of inaccurate, absent or noisy vestibular or somatosensory information or both, or even a potential issue
with conflict between the two system’s information. Therefore, although the Romberg is likely the quickest and easiest test of potential balance dysfunction (likely why it is commonplace), it is also the most limited in its interpretation of potential underlying mechanisms contributing to balance dysfunction.27 Finally, no known reliability or validity data exist to support the Romberg test for use in concussion populations. In response to continued issues of practicality, expense, and sensitivity, researchers at the University of North Carolina developed the Balance Error Scoring System (BESS).7–9 The BESS is being increasingly used in the clinical assessment of balance in patients with a potential concussion injury. Its development was based on the underlying principles of the Romberg, SOT, and CTSIB tests. The BESS differs from the other static standing balance tests is
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In summary, although standing static balance tests are used commonly for assessing balance postconcussion, no single test provides optimal information regarding postconcussion balance deficits. Use of a particular test is likely a result of the equipment and time available, and it is essential for clinicians to consider the limitations of a given test when interpreting results.
IMPORTANT CONSIDERATIONS WHEN ASSESSING BALANCE IN ADULTS WITH CONCUSSION When observing results from balance tests, clinicians need to keep in mind a few points. One of the major criticisms for the static tests currently used in the assessment of balance dysfunction postconcussion is that they lack sensitivity to detect deficits in postural control. The lack of sensitivity has two major factors: (1) measurement sensitivity and (2) the nature of the test. The first issue of sensitivity, measurement sensitivity, is that most of the standing balance tests depend on some measure of magnitude or presence of sway, and although increased magnitude in sway can be indicative of postural difficulties, it is not always the case. In some populations, increased magnitude of sway is attributed to postural control strategies used to enhance learning and adaptation of perception-action relationships.2,34,35 Given that athletes capitalize on their ability to adapt perception and action, athletes may tend to show greater postural sway than a nonathlete.34 As such, use of a measure of the magnitude of sway, particularly when compared with a normative database and not an athlete’s own baseline, may create false-positives in diagnosing the presence of balance dysfunction. Therefore, when interpreting increased sway as a deficit in balance, particularly when used in isolation, caution must be used as it may not reflect a balance deficit but rather a healthy adaptive learning system. To address this limitation, the use of additional measures of postural control is desirable. One such measure is sway velocity. In postural control literature, velocity is a measure of underlying motor control strategies to maintain upright stance. Greater velocities and the number of excursions indicate greater
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that it does not compare the difference in postural control under different visual conditions (Fig. 1). Patients are required to close their eyes for all conditions and place their hands on their hips. Patients are then asked to stand for 20 seconds in three different positions (singleleg stance, feet together, and heel to toe) on two different surfaces (firm and foam).9,28 Assessment of postural stability is defined as the sum of errors observed during the trials from a list of six potential errors including removing the hands from the hips, opening the eyes, and stepping or stumbling. Although the number of errors is certainly quantitative, the BESS suffers from the same criticism as the CTSIB, in that its sensitivity may limit its ability to detect deficits in spontaneous sway. This is because errors are determined by rater observation. Despite this potential limitation, interrater and intrarater reliability of the BESS is moderate to good with variance in reliability between different stance position subscores as well as the total test score when assessing healthy young adults and athletes.26,28 For a systematic review of the reliability of the BESS see Bell et al.26 One potential further limitation to the BESS in assessment of concussion is that there have been reported learning effects with the test, potentially raising a concern for use in athletic populations that are likely proficient at learning motor tasks.29 Improvements in performance on the BESS as a result of motor learning rather than recovery from the injury could result in undervaluation of balance impairments and premature return to play. Finally, the most recent addition to potential balance tests recommended for use in concussion assessment is the Nintendo WiiFit (Nintendo Co., Ltd., Kyoto, Japan). Rationale for the use of the Wii is that it can serve as an inexpensive substitute for a force platform and measure COP information if used with the Wii Balance Board. However, although COPs obtained from the Wii provide fairly good comparisons to those obtained with research-grade force platforms,30,31 the Wii has yet to be validated for its ability to detect balance deficits.32,33 Therefore, use of the Wii as a balance assessment tool must be approached with caution and should not be used in exclusion of other tests of balance function.
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spontaneity of sway and reduced control over the pattern of movements. One further issue with measurement sensitivity of balance tests in detecting deficits in balance postconcussion is that of variability. Although several studies have examined the reliability of balance tests for assessment of balance dysfunction postconcussion, they have reported high variability among trials and conditions.6,14 However, it is not clear whether this should be a concern or not. One potential consideration is that variability can be both a sign of a healthy motor control system and an unhealthy one.37 Recording the variability of patients on balance tests could provide an additional way to monitor progress, particularly if on average the patient tends to have normative scores. The degree of variability may indicate that there are still some residual effects of a concussion injury on the neurologic system. The second issue with sensitivity of static balance tests is the nature of the tests. Standing balance tests are simple and static and do not represent the complexity of motor control or postural control required in a sport environment. Support for this argument has come from studies that have evaluated postural control using complex movements such as obstacle avoidance during gait in both single- and dual-task paradigms, as well as postural control during stance under dynamic control. Slobonouv et al (2008)14 studied postural control postconcussion using both static eyes open and eyes closed standing balance (similar to a Romberg test) and under a standing balance task where the participant was required to actively sway back and forth at a self-selected speed to the limits of their own boundary of stability. These authors used a novel method to measure COP, in addition to traditional measures such as velocity and magnitude of COP. They found abnormalities in postural control up to 30 days after concussion injury although function on standard clinical tests had already returned to normal and the participants had returned to play. These results suggest that by having the subjects oscillate, introducing a greater number of control parameters for stance such as anticipatory postural adjustments, significant differences were observed between a group of participants with concussions and those without. These findings support the arguments for
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the need for variables that are more sensitive and tasks that are more complex in the assessment of balance in concussion. Continued abnormalities in postural control that are missed on traditional static tests could leave the athlete vulnerable for further injury. Parker and colleagues used a dual-task paradigm to assess dynamic postural stability during gait postconcussion.15 These authors evaluated a group of athletes with concussion from 48 hours postinjury to 5, 14, and 28 days postinjury on level walking under single-task conditions (gait task) and dual-task conditions (secondary cognitive task). They found that while significant differences on gait parameters between the concussion group and a control group were evident at days 2 and 5 when participants performed the single task of walking, significant differences in performance were present in dual-task walking up to 28 days postconcussion. Catena and colleagues (2009)39 also studied dual-task performance during gait tasks, including obstacle avoidance, in participants postconcussion compared with controls. Similar to Parker and colleagues,15 Catena et al found that participants with concussion were more cautious in their gait patterns and had significantly worse performance on the dual cognitive task compared with the control group. These results have substantial implications for return to play as they indicate that although primary motor task performance may recover quickly following injury, the ability to perform a concurrent cognitive task with a motor task remains deficient. Considering that athletic events require both physical and mental performance, it is likely that deficits in dual-task performance are an important consideration to decisions about returning to play. As a result, use of dual-task paradigms may provide a valuable addition to current tests of postural control and balance and done without additional time or expense.
THE FUTURE OF BALANCE ASSESSMENT IN CONCUSSION Sideline Versus Clinical One major issue that has driven the use of one particular balance test over others has been the
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practicality of tests and their feasibility of use on the sideline. It is a delicate issue, where sacrifices in the sophistication and sensitivity of tests are made for simplicity and speed. However, one of the important points to keep in mind when assessing balance is that depending on the underlying mechanisms at work in concussion (e.g., edema or adaptation by the CNS), balance dysfunction may not present immediately. Indeed, there is a developing emphasis that a concussion is an evolving injury where signs and symptoms may not appear immediately after injury.38 The latest consensus statement on concussion in sport recommends the use of balance as a component of sideline tests to help health professionals determine whether a concussion has occurred.38 However, it remains to be determined if sideline tests should influence how balance assessment is conducted in a clinical setting, specifically as space, time, and equipment is more readily available. Perhaps tests used in the clinic moving the sideline should have different goals. Tests in the clinic moving away from those advantageous for the sideline to those advantageous for detecting the recovery of function for more effective returnto-play decisions. The future of concussion diagnosis via sideline balance assessment may rest in the hands of mobile software and hardware developers. With the increasing capacity of mobile technology, the ability of medical personnel to quickly and quantitatively assess balance in an individual with a suspected concussion is growing. One example of this development using existing technology is the interaction of Wii Balance Boards with mobile technology. As previously presented, the Wii Balance Board has been accepted as a surrogate method of recording COP data; however, among other limitations, its sideline use is limited by the need for a power supply and monitor. In response to this, emerging software can connect the Bluetooth Wii Balance Board to a mobile device such as a tablet or mobile phone, allowing for quantitative assessment of balance to be conducted. In such a case, each of the COPbased measures of postural stability could be assessed in near-real time to guide sideline decision making pertaining to the health of the athlete.
However, as it has been demonstrated that the assessment of quiet, static standing trials may not be sufficient to determine the presence or absence of concussion, the development of mobile software to assess more dynamic tasks for concussion testing should be developed. A potential application of existing technology to assess concussion using a gait task could be the use of a waist-mounted system capable of tracking step time, length, and frequency as well as gait asymmetry. This novel application of existing technology could provide insight into the health of the neuromuscular system using a dynamic/gait task.
Recommendations on Best Practices Current clinical balance assessments used in the diagnosis and rehabilitation of concussion injury use the quiet static standing position.8 For example, the Romberg test and the BESS require that the person remain as still as possible in an upright position during evaluation in an unmoving environment. As such, these tests attempt to describe postural control based on little to no external stimulation and as a result may not adequately describe functional balance problems exhibited after a concussion injury.13–15,19,21,39 During a dynamic task, in a rapidly changing environment, the CNS must weigh incoming multimodal sensory information, perceive that information in relevance to the situation, and apply previous experience and training to a motor plan to regulate postural control. These situations are both physically and cognitively demanding and emulate a level of control required in sports. Therefore, balance tests using dynamic tasks in a changing environment may expose functional deficits that are not evident from static postural tests. For an athlete returning to competitive play, dynamic tasks relevant to their sporting environment may pose a greater advantage in the determination of return to play. In summary, most studies that have observed postural control beyond 3 to 5 days postinjury have used laboratory-based testing and sophisticated equipment. This has likely been the barrier for and the reason why few clinics have adopted these methodologies, despite the evidence that these tests and methods
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may provide greater insight into recovery and potentially better estimates of recovery of function. There is clearly a need for translation of this research to the clinics. COP is not a difficult measure to understand or measure, and applying a variety of algorithms to quantitatively assess balance using COP is not timeconsuming given current computer processing capabilities. In the case of motor task complexity, even a simple dual cognitive task during clinical balance testing may increase the sensitivity of the test to the presence of motor control deficits. Therefore, as concussion is an evolving injury, perhaps a progressive approach to balance assessment is required. As far as a best practice to balance assessment, there is clearly no single “best” test for balance assessment in concussion. The judicious decision ultimately lies with the clinician. It is, therefore, the responsibility of the clinician to stay current with developments in balance assessment in concussion. It may be best practice for clinicians that assess balance in concussion to use multiple tests and approaches. As of the current state of knowledge, use of a validated balance test such as the BESS, with perhaps an additional battery under dual-task conditions, may be beneficial. Alternatively, the use of two assessments, one standing and one dynamic, such as the BESS and a gait task, may provide greater insight into deficits in the underlying motor control. Given this, the takehome message for any clinician assessing balance in concussion is that the use of a single test exclusively may hinder efforts to effectively determine the presence of an injury and recovery.
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BALANCE IN ADULTS WITH CONCUSSION/REED-JONES ET AL
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ABSTRACT
Balance is a key component to the assessment of concussion injury; however, the efficacies of clinical tests used are currently under debate. It is questionable whether currently accepted methods of standing balance assessment quantify balance disturbances sufficiently to support decisions on recovery and return to play. Recent evidence of balance abnormalities postconcussion that linger beyond the typical 3to 5-day recovery period support arguments that currently available standing balance tests are not sensitive enough to determine recovery of function. This article discusses the current clinical tests used in the assessment of concussion in adults and their limitations and the evidence supporting continued balance dysfunction. Implications for the future of balance assessment in concussed adults and recommendations to clinicians for best practices are presented. KEYWORDS: Balance assessment, standing balance, vestibular,
sensory integration, concussion
Learning Outcomes: As a result of this activity, the reader will be able to (1) discuss the underlying mechanisms of balance control and the effects of concussion on these mechanisms; (2) summarize the current methods for balance assessment and their limitations; (3) discuss the implications of current evidence supporting lingering balance issues postconcussion; (4) apply the current state of knowledge of balance postconcussion to best practices when assessing concussion in adults.
1
Department of Applied Human Sciences, Faculty of Science, University Prince Edward Island, Charlottetown, Prince Edward Island, Canada; 2Interdisciplinary Health Sciences Ph.D. Program, University of Texas at El Paso, El Paso, Texas; 3Department of Physical Therapy, Campbell University, Buies Creek, North Carolina. Address for correspondence: Rebecca J. Reed-Jones, Ph.D., Department of Applied Human Sciences, Faculty of Science, University Prince Edward Island, 550 University
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Avenue, Charlottetown, PE, Canada, C1A 4P3 (e-mail: [email protected]). Concussion 101 for SLPs; Guest Editor, Anthony P. Salvatore, Ph.D., CCC-SLP Semin Speech Lang 2014;35:186–195. Copyright # 2014 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA. Tel: +1(212) 5844662. DOI: http://dx.doi.org/10.1055/s-0034-1384680. ISSN 0734-0478.
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Rebecca J. Reed-Jones, Ph.D.,1 Nicholas G. Murray, Ph.D.,2 and Douglas W. Powell, Ph.D.3
WHY BALANCE IS AN IMPORTANT COMPONENT OF CLINICAL ASSESSMENT OF CONCUSSION Balance is a dynamic action requiring control of the effects of gravity on the body. In bipedal quiet stance, humans are never motionless; small excursions or an observed sway occur and are a reflection of fine adjustments made by the muscles about the joints to continue alignment with gravitational forces.1 The motor control system receives information regarding the required magnitude and location of adjustments through the sensation and perception of orientation, position, and motion of the body and its segments by the sensory systems.2 As such, even the simple task of standing with 2 feet in upright stance requires integration of sensation, perception, and motor coordination. Any disruption within these processes can result in muscular maladjustments and result in inconsistent sway patterns. These abnormal sway patterns are the focus of balance assessment following a concussion.
WHAT OCCURS TO BALANCE CONTROL POSTCONCUSSION Balance disturbances occur in up to 80% of sport-related concussion injuries, with dizziness occurring in 75.6% of injuries.3,4 The most commonly measured balance variable is the presence or absence of increased sway and/or the magnitude of sway movement. The presence of increased sway is interpreted as a decrease in balance control. Measuring sway postconcussion using a quiet upright bipedal stance or static method suggests that a dysfunction of balance is greatest at 1 day postconcussion. Furthermore, the literature suggests that this dysfunction resolves within 3 to 5 days postconcussion. The recovery of balance also apparently precedes the recovery of cognitive performance and a decrease in postconcussion symptoms.5–10 However, there is increasing evidence to suggest that balance dysfunction can persist for weeks, months, and even years following a concussion.3,11–15 Although these data are based upon the use of static measures of balance, abnormal postural control has been demonstrated up to 30 days postinjury using dynamic balance and gait tasks.13,14 For a
summary of studies examining the resolution of balance dysfunction postconcussion, see Table 1. An important consideration regarding the differences in postural control recovery between static standing balance tests and dynamic balance/gait tests is that the traditional reliance upon static standing balance tests alone may result in a premature return-to-play decision. Such a premature decision may place an individual at greater risk for falling and/or collisions during play, as well as during activities of daily living. Therefore, susceptibility to a second concussion event is increased across all activities.
HYPOTHESIZED UNDERLYING MECHANISMS THAT ARE DISRUPTED DUE TO CONCUSSION Sensory information received from the visual system, the somatosensory system, and the vestibular system all contribute to the control of balance. Of the three sensory systems, the vestibular system may be a primary contributor to balance disruptions following concussion.6,8,12,16,17 The vulnerability of the vestibular system to damage following a concussion is certainly plausible; impacts in the cranial area can disturb the sensitive hair cells and interfere with sensation. However, the potential for physical damage sustained by the vestibular system from concussion injuries is still largely unknown. Another explanation regarding disruption of vestibular information suggests that axonal injury and edema caused by the impact interrupts vestibular afferents to the brain.18 Acute disruptions to afferent signals could explain the high incidence of dizziness and the loss of balance control within the first 24 hours following injury. Resolution of edema following injury could also explain gross recovery of balance within 72 hours postinjury. However, persistent balance issues indicate the potential for mechanisms beyond disruption due to edema. Recent studies support the hypothesis that a dysfunction in the control mechanisms of posture occurs at the sensory integration level.19,20 The central nervous system (CNS) may filter or reweight vestibular information during the acute recovery phase based on erroneous or
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BALANCE IN ADULTS WITH CONCUSSION/REED-JONES ET AL
during CTSIB BESS and SOT BESS BESS ApEn algorithm to COP
and high school)
16 athletes age 19.2 2.3 y 94 collegiate football players
570 football players
(collegiate and high school) 29 collegiate athletes
8 collegiate athletes
38 collegiate athletes
15 collegiate athletes
Riemann et al (2000)9 McCrea at el (2003)5
McCrea et al (2012)10
Cavanaugh et al (2006)16
Slobounov et al (2006)13
Slobounov et al (2008)14
Parker et al (2006)15 Up to 28 d
No, symptoms resolved earlier
No, symptoms resolved earlier
NA
No, symptoms resolved earlier
No, balance resolved earlier
Yes Yes
NA
Relation to Symptom Resolution
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Note: Top four studies used standard balance tests. Bottom four studies used novel approaches to balance assessment. Abbreviations: ApEn, approximate entropy; BESS, Balance Error Scoring System; COP, center of pressure; CTSIB, Clinical Test of Sensory Interaction and Balance; NA, not available; SOT, Sensory Organization Test.
dual-task level walking
Up to 30 d
COP from dynamic bal-
Up to 30 d
Up to 96 h
Up to 3 h postinjury
Up to 3 d Resolve 3–5 d
Up to 3–5 d
Significant Effects Present Postinjury
ance task Kinematics during single/
COP of standing balance during visual field motion
from SOT
Sway magnitude of COP
10 football players (collegiate
Guskiewicz et al (1996)6
Test
Population with Concussion
Summary of Studies Examining Recovery of Balance Postconcussion
Study
Table 1
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noisy sensory information derived from a damaged organ or disrupted afferent function due to edema.19–21 On resolution of vestibular information, the CNS must correctly reintegrate incoming vestibular sensory information with visual and somatosensory information. How and when the CNS does this following a concussion injury is still largely unknown and, therefore, could be a potential mechanism for continued balance dysfunction. However, without the use of brain imaging or direct measurements of the brain, this observation is speculative. To date, no literature has examined or observed direct damage to either the vestibular organs or vestibular nuclei. Until direct measurements occur, indirect measurements must suffice to rule out the contributions of the vestibular system to balance dysfunction after a concussion episode.
CURRENT TESTS USED TO ASSESS CONCUSSION The most commonly used tests to assess balance postconcussion are the Sensory Organization Test (SOT),22 the Clinical Test of Sensory Integration and Balance,23 the Romberg test,24,25 and the Balance Error Scoring System.9,26 These tests assess static standing balance control under varying sensory conditions. For a more exhaustive comparison of these tests in the assessment of concussion, see Guskiewicz.8 The SOT and Clinical Test of Sensory Interaction and Balance (CTSIB) were developed to assess contributions of the sensory systems to postural control. They are presented together because their procedures and interpretations are similar with CTSIB being a simpler and more inexpensive version of the SOT. The SOT was developed as a tool to examine the contributions of each sensory system to postural control as well as the adaptability of the CNS to select and use the most relevant sensory information.22 Therefore, the SOT not only provides insight into each system’s use but also provides insight into the effectiveness of the CNS to interpret and respond to erroneous information. The SOT apparatus consists of two moveable instrumented platforms that rotate and translate independently. The first platform contains the
support surface on which the patient stands. The second platform is composed of a visual surface that rotates about an axis that is colinear with the patient’s ankles and produces visual perturbations to the patient’s visual reference frame.22 Postural control assessment using the SOT is composed of an objective measurement of center of pressure (COP) path by a force platform. A force platform is an instrumented plate that records forces produced by an individual standing on the plate. COP is a measure derived from these forces and, as the name infers, is the center (or concentration) of these forces. The pattern of movement of the COP is a direct result of movements of the body on the plate. As such, it is an objective measure of balance. Measures of sway of the body’s center of mass can also be measured using a potentiometer attached at the hips. Since the development of this protocol, the apparatus of the SOT has been developed in a commercially available product, NeuroCom’s EquiTest (NeuroCom1 a division of Natus, Clackamas, OR). To address the issue of the practicality and expense of the apparatus in clinical settings Shumway-Cook and Horak developed the CTSIB.23 The CTSIB also has six conditions (three visual conditions and three surface conditions) for assessing a patient’s postural control (Fig. 1). The difference from the SOT is that the CTSIB uses foam under the feet to manipulate somatosensory information and a paper lantern placed over the head to manipulate visual references. These modifications allow the CTSIB to be less expensive. Assessment is composed of three measures: (1) the amount of time a patient can maintain stance, (2) a subjective assessment ranking the magnitude of sway observed in each condition, and (3) objective measurement of the body’s displacement via a plum line attached to the body. Studies have also used a force plate to objectively measure COP during these conditions.6 The benefit of both the SOT and CTSIB are that the results provide insight into which sensory system a patient relies on for postural control. The Romberg test is perhaps the oldest and most commonly used clinical test of postural control. The test itself is simple and requires a patient to stand first with the eyes open and then with the eyes closed. Standing can be done
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Figure 1 Comparison of sensory conditions of the Sensory Organization Test (SOT), Clinical Test of Sensory Integration and Balance (CTSIB), and Balance Error Scoring System (BESS). Note that the sensory manipulations in the SOT and CTSIB are identical, despite the different methods to produce the manipulations. The BESS is a simplification, including only conditions 2 and 5 of the SOT and CTSIB. The major difference is that the BESS has three stance configurations for each sensory condition, two feet, single foot, and heel-totoe stance (not represented in the figure).
in several different configurations; the most common configuration is feet together; however, tandem stance (heel to toe) can also be used and is a more challenging test.25 Typically, the Romberg test is a positive or negative rating, with a positive rating given when increased sway (e.g., magnitude and/or velocity) is observed when the eyes are closed.27 The Romberg test provides insight into whether somatosensory and vestibular sensory information are providing sufficient information to maintain stance. When a positive sign is present, at least one of the remaining sensory systems is contributing to inappropriate postural adjustments. However, the test is limited in any further interpretation to what is occurring within those two sensory systems. A positive Romberg could be the result of inaccurate, absent or noisy vestibular or somatosensory information or both, or even a potential issue
with conflict between the two system’s information. Therefore, although the Romberg is likely the quickest and easiest test of potential balance dysfunction (likely why it is commonplace), it is also the most limited in its interpretation of potential underlying mechanisms contributing to balance dysfunction.27 Finally, no known reliability or validity data exist to support the Romberg test for use in concussion populations. In response to continued issues of practicality, expense, and sensitivity, researchers at the University of North Carolina developed the Balance Error Scoring System (BESS).7–9 The BESS is being increasingly used in the clinical assessment of balance in patients with a potential concussion injury. Its development was based on the underlying principles of the Romberg, SOT, and CTSIB tests. The BESS differs from the other static standing balance tests is
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BALANCE IN ADULTS WITH CONCUSSION/REED-JONES ET AL
In summary, although standing static balance tests are used commonly for assessing balance postconcussion, no single test provides optimal information regarding postconcussion balance deficits. Use of a particular test is likely a result of the equipment and time available, and it is essential for clinicians to consider the limitations of a given test when interpreting results.
IMPORTANT CONSIDERATIONS WHEN ASSESSING BALANCE IN ADULTS WITH CONCUSSION When observing results from balance tests, clinicians need to keep in mind a few points. One of the major criticisms for the static tests currently used in the assessment of balance dysfunction postconcussion is that they lack sensitivity to detect deficits in postural control. The lack of sensitivity has two major factors: (1) measurement sensitivity and (2) the nature of the test. The first issue of sensitivity, measurement sensitivity, is that most of the standing balance tests depend on some measure of magnitude or presence of sway, and although increased magnitude in sway can be indicative of postural difficulties, it is not always the case. In some populations, increased magnitude of sway is attributed to postural control strategies used to enhance learning and adaptation of perception-action relationships.2,34,35 Given that athletes capitalize on their ability to adapt perception and action, athletes may tend to show greater postural sway than a nonathlete.34 As such, use of a measure of the magnitude of sway, particularly when compared with a normative database and not an athlete’s own baseline, may create false-positives in diagnosing the presence of balance dysfunction. Therefore, when interpreting increased sway as a deficit in balance, particularly when used in isolation, caution must be used as it may not reflect a balance deficit but rather a healthy adaptive learning system. To address this limitation, the use of additional measures of postural control is desirable. One such measure is sway velocity. In postural control literature, velocity is a measure of underlying motor control strategies to maintain upright stance. Greater velocities and the number of excursions indicate greater
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that it does not compare the difference in postural control under different visual conditions (Fig. 1). Patients are required to close their eyes for all conditions and place their hands on their hips. Patients are then asked to stand for 20 seconds in three different positions (singleleg stance, feet together, and heel to toe) on two different surfaces (firm and foam).9,28 Assessment of postural stability is defined as the sum of errors observed during the trials from a list of six potential errors including removing the hands from the hips, opening the eyes, and stepping or stumbling. Although the number of errors is certainly quantitative, the BESS suffers from the same criticism as the CTSIB, in that its sensitivity may limit its ability to detect deficits in spontaneous sway. This is because errors are determined by rater observation. Despite this potential limitation, interrater and intrarater reliability of the BESS is moderate to good with variance in reliability between different stance position subscores as well as the total test score when assessing healthy young adults and athletes.26,28 For a systematic review of the reliability of the BESS see Bell et al.26 One potential further limitation to the BESS in assessment of concussion is that there have been reported learning effects with the test, potentially raising a concern for use in athletic populations that are likely proficient at learning motor tasks.29 Improvements in performance on the BESS as a result of motor learning rather than recovery from the injury could result in undervaluation of balance impairments and premature return to play. Finally, the most recent addition to potential balance tests recommended for use in concussion assessment is the Nintendo WiiFit (Nintendo Co., Ltd., Kyoto, Japan). Rationale for the use of the Wii is that it can serve as an inexpensive substitute for a force platform and measure COP information if used with the Wii Balance Board. However, although COPs obtained from the Wii provide fairly good comparisons to those obtained with research-grade force platforms,30,31 the Wii has yet to be validated for its ability to detect balance deficits.32,33 Therefore, use of the Wii as a balance assessment tool must be approached with caution and should not be used in exclusion of other tests of balance function.
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spontaneity of sway and reduced control over the pattern of movements. One further issue with measurement sensitivity of balance tests in detecting deficits in balance postconcussion is that of variability. Although several studies have examined the reliability of balance tests for assessment of balance dysfunction postconcussion, they have reported high variability among trials and conditions.6,14 However, it is not clear whether this should be a concern or not. One potential consideration is that variability can be both a sign of a healthy motor control system and an unhealthy one.37 Recording the variability of patients on balance tests could provide an additional way to monitor progress, particularly if on average the patient tends to have normative scores. The degree of variability may indicate that there are still some residual effects of a concussion injury on the neurologic system. The second issue with sensitivity of static balance tests is the nature of the tests. Standing balance tests are simple and static and do not represent the complexity of motor control or postural control required in a sport environment. Support for this argument has come from studies that have evaluated postural control using complex movements such as obstacle avoidance during gait in both single- and dual-task paradigms, as well as postural control during stance under dynamic control. Slobonouv et al (2008)14 studied postural control postconcussion using both static eyes open and eyes closed standing balance (similar to a Romberg test) and under a standing balance task where the participant was required to actively sway back and forth at a self-selected speed to the limits of their own boundary of stability. These authors used a novel method to measure COP, in addition to traditional measures such as velocity and magnitude of COP. They found abnormalities in postural control up to 30 days after concussion injury although function on standard clinical tests had already returned to normal and the participants had returned to play. These results suggest that by having the subjects oscillate, introducing a greater number of control parameters for stance such as anticipatory postural adjustments, significant differences were observed between a group of participants with concussions and those without. These findings support the arguments for
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the need for variables that are more sensitive and tasks that are more complex in the assessment of balance in concussion. Continued abnormalities in postural control that are missed on traditional static tests could leave the athlete vulnerable for further injury. Parker and colleagues used a dual-task paradigm to assess dynamic postural stability during gait postconcussion.15 These authors evaluated a group of athletes with concussion from 48 hours postinjury to 5, 14, and 28 days postinjury on level walking under single-task conditions (gait task) and dual-task conditions (secondary cognitive task). They found that while significant differences on gait parameters between the concussion group and a control group were evident at days 2 and 5 when participants performed the single task of walking, significant differences in performance were present in dual-task walking up to 28 days postconcussion. Catena and colleagues (2009)39 also studied dual-task performance during gait tasks, including obstacle avoidance, in participants postconcussion compared with controls. Similar to Parker and colleagues,15 Catena et al found that participants with concussion were more cautious in their gait patterns and had significantly worse performance on the dual cognitive task compared with the control group. These results have substantial implications for return to play as they indicate that although primary motor task performance may recover quickly following injury, the ability to perform a concurrent cognitive task with a motor task remains deficient. Considering that athletic events require both physical and mental performance, it is likely that deficits in dual-task performance are an important consideration to decisions about returning to play. As a result, use of dual-task paradigms may provide a valuable addition to current tests of postural control and balance and done without additional time or expense.
THE FUTURE OF BALANCE ASSESSMENT IN CONCUSSION Sideline Versus Clinical One major issue that has driven the use of one particular balance test over others has been the
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practicality of tests and their feasibility of use on the sideline. It is a delicate issue, where sacrifices in the sophistication and sensitivity of tests are made for simplicity and speed. However, one of the important points to keep in mind when assessing balance is that depending on the underlying mechanisms at work in concussion (e.g., edema or adaptation by the CNS), balance dysfunction may not present immediately. Indeed, there is a developing emphasis that a concussion is an evolving injury where signs and symptoms may not appear immediately after injury.38 The latest consensus statement on concussion in sport recommends the use of balance as a component of sideline tests to help health professionals determine whether a concussion has occurred.38 However, it remains to be determined if sideline tests should influence how balance assessment is conducted in a clinical setting, specifically as space, time, and equipment is more readily available. Perhaps tests used in the clinic moving the sideline should have different goals. Tests in the clinic moving away from those advantageous for the sideline to those advantageous for detecting the recovery of function for more effective returnto-play decisions. The future of concussion diagnosis via sideline balance assessment may rest in the hands of mobile software and hardware developers. With the increasing capacity of mobile technology, the ability of medical personnel to quickly and quantitatively assess balance in an individual with a suspected concussion is growing. One example of this development using existing technology is the interaction of Wii Balance Boards with mobile technology. As previously presented, the Wii Balance Board has been accepted as a surrogate method of recording COP data; however, among other limitations, its sideline use is limited by the need for a power supply and monitor. In response to this, emerging software can connect the Bluetooth Wii Balance Board to a mobile device such as a tablet or mobile phone, allowing for quantitative assessment of balance to be conducted. In such a case, each of the COPbased measures of postural stability could be assessed in near-real time to guide sideline decision making pertaining to the health of the athlete.
However, as it has been demonstrated that the assessment of quiet, static standing trials may not be sufficient to determine the presence or absence of concussion, the development of mobile software to assess more dynamic tasks for concussion testing should be developed. A potential application of existing technology to assess concussion using a gait task could be the use of a waist-mounted system capable of tracking step time, length, and frequency as well as gait asymmetry. This novel application of existing technology could provide insight into the health of the neuromuscular system using a dynamic/gait task.
Recommendations on Best Practices Current clinical balance assessments used in the diagnosis and rehabilitation of concussion injury use the quiet static standing position.8 For example, the Romberg test and the BESS require that the person remain as still as possible in an upright position during evaluation in an unmoving environment. As such, these tests attempt to describe postural control based on little to no external stimulation and as a result may not adequately describe functional balance problems exhibited after a concussion injury.13–15,19,21,39 During a dynamic task, in a rapidly changing environment, the CNS must weigh incoming multimodal sensory information, perceive that information in relevance to the situation, and apply previous experience and training to a motor plan to regulate postural control. These situations are both physically and cognitively demanding and emulate a level of control required in sports. Therefore, balance tests using dynamic tasks in a changing environment may expose functional deficits that are not evident from static postural tests. For an athlete returning to competitive play, dynamic tasks relevant to their sporting environment may pose a greater advantage in the determination of return to play. In summary, most studies that have observed postural control beyond 3 to 5 days postinjury have used laboratory-based testing and sophisticated equipment. This has likely been the barrier for and the reason why few clinics have adopted these methodologies, despite the evidence that these tests and methods
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may provide greater insight into recovery and potentially better estimates of recovery of function. There is clearly a need for translation of this research to the clinics. COP is not a difficult measure to understand or measure, and applying a variety of algorithms to quantitatively assess balance using COP is not timeconsuming given current computer processing capabilities. In the case of motor task complexity, even a simple dual cognitive task during clinical balance testing may increase the sensitivity of the test to the presence of motor control deficits. Therefore, as concussion is an evolving injury, perhaps a progressive approach to balance assessment is required. As far as a best practice to balance assessment, there is clearly no single “best” test for balance assessment in concussion. The judicious decision ultimately lies with the clinician. It is, therefore, the responsibility of the clinician to stay current with developments in balance assessment in concussion. It may be best practice for clinicians that assess balance in concussion to use multiple tests and approaches. As of the current state of knowledge, use of a validated balance test such as the BESS, with perhaps an additional battery under dual-task conditions, may be beneficial. Alternatively, the use of two assessments, one standing and one dynamic, such as the BESS and a gait task, may provide greater insight into deficits in the underlying motor control. Given this, the takehome message for any clinician assessing balance in concussion is that the use of a single test exclusively may hinder efforts to effectively determine the presence of an injury and recovery.
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BALANCE IN ADULTS WITH CONCUSSION/REED-JONES ET AL
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