Figure 1: Structure of a typical neuron

Diffuse axonal injury can be present at a remote site such as the brain-stem and cerebellum, where integrators for the vestibular and oculomotor nuclei converge.  If a second insult to the brain occurs during the energy-failure of a previous injury, the results can lead to irreversible neuronal injury and massive cell death.

These cascading neurochemical events are a logical explanation for the transient and prolonged symptoms of concussion.  Prolonged pathophysiological changes that affect neurotransmission are likely to decrease the effectiveness of synaptic plasticity via protein expression, potentially hindering the effectiveness of ill-timed rehabilitation (MacFarlane and Glenn, 2015).

It has been proposed that not only are there local changes at the level of the brain but also immediate change to the gut following injury.  This link between gut and brain is bidirectional, with the brain influencing the enteric nervous system and vice versa, creating complex neuro-inflammatory and neuro-immunological loops (Kharrazian, 2015).

Animal studies have shown that gut bacteria are disrupted within hours of a head injury.  The gut microbiome is involved in multiple processes critical to the progression of TBI, with links to “neuroinflammation, blood-brain barrier permeability, immune system response, microglial activation, and mitochondrial dysfunction, as well as intestinal motility and permeability” (Rice, Pandya and Shear, 2019).

The link between gut and brain poses the question around gut-related interventions for concussion, however, this is beyond the scope of this discussion.

Assessment of concussion

Whenever a head injury has occurred, the initial concern is around the possibility of an epidural or subdural haematoma, parenchymal haemorrhage or increased intracranial pressure.  If there is a reason to suspect severe brain or neck injury, emergent evaluation is indicated.

Figure 2: Epidural vs Subdural heamatoma

If sinister injury is not suspected there are some key questions to consider:

• what impairments have occurred because of the injury?
• what is the best way to assess and measure the current impairments?
• when is the best time to return to sport?

But with such a wide variety of potential neurological impairments and symptoms the answers to these questions can become complex, hence, standardised assessment protocols are required.

One of the most commonly used and widely recognized tools for evaluating concussions in sport, is the Sports Concussion Assessment Tool, 5^th Ed (SCAT 5).  This series of examinations, developed by the CISG experts, is widely accepted as a very useful side-line tool for immediately distinguishing concussed versus non-concussed athletes (McCrory et al., 2017).

The SCAT5 assessment covers a variety of neurological assessments including observation, cognitive, physical and balance assessments.  More specifically, the consensus is that:

“the suspected diagnosis of sports-related concussion can include one or more of the following clinical domains”:

1. Symptoms: somatic (eg, headache), cognitive (eg, feeling like in a fog) and/or emotional symptoms (eg, lability)
2. Physical signs (eg, loss of consciousness, amnesia, neurological deficit)
3. Balance impairment (eg, gait unsteadiness)
4. Behavioural changes (eg, irritability)
5. Cognitive impairment (eg, slowed reaction times)
6. Sleep/wake disturbance (eg, somnolence, drowsiness)”

The conference consensus goes on to “recommended that all athletes should have a clinical neurological assessment (including evaluation of mental status/cognition, oculomotor function, gross sensorimotor, coordination, gait, vestibular function and balance) as part of their overall management” (McCrory et al., 2017).

As a first-response tool, the SCAT5 remains a very practical and easily accessible option for enabling trained medical practitioners the ability to carry out multi-modal testing with nothing more than a pen and paper.  However, because its utility is significantly less after 3-5 days’ post-injury, it is recommended that a more detailed and sensitive battery of assessments are used to distinguish ongoing levels of impairment.

It should also be noted that, although the CISG recommends oculomotor and vestibular testing as part of the comprehensive assessment, the SCAT-5 approach to concussion detection does not specifically nor objectively test oculomotor and vestibular function (Hunfalvay et al., 2020).  To do so requires expensive equipment and time-consuming assessments, all of which are impractical for side-line applications.

In a study titled “Current and emerging rehabilitation for concussion”, published in 2015, a clinical model of sports-related concussion is proposed.   Based on the finding that oculomotor and vestibular subtypes are associated with poor clinical outcomes, researchers have suggested the identification of clinical subtypes along with the application of targeted therapies to yield the most effective outcomes for athletes.  It goes on to suggest that without such targeted strategies, “an athlete may experience an unnecessarily prolonged recovery from SRC” (Broglio et al., 2015).

In agreeance with the advice of the CISG are the separate but more recent recommendations coming from a meta-analysis of literature released by the Stanford University (Lumba-Brown et al., 2019).  This study also concludes that a comprehensive evaluation of acute concussion should include assessments for subtypes and associated conditions. According to the study, whereby a meta-analysis was performed of over 3000 records published between 1990 and 2017, there can be five subtypes of concussion classified, including: 

1. Cognitive
2. Headache migraine
3. Oculomotor
4. Vestibular
5. Anxiety / mood

As well as two concussion-associated conditions:

1. Sleep disturbance
2. Cervical strain

Figure 3a: Subtypes of concussion (Lumba-Brown et al., 2019).

Figure 4: Prevalence of concussion subtypes and sleep disturbances in concussion patients (Lumba-Brown et al., 2019).

With such a variety of potential symptoms and subtypes, it is recommended that a subjective score is obtained from the concussed patient. The Rivermead post-concussion questionnaire can help categorize the symptoms of each subtype and therefore can be used both as a standardized subjective measurement tool and a guideline towards intervention requirements (Maruta, Lumba-Brown and Ghajar, 2018). It should be remembered that the Rivermead questionnaire scores on their own are not diagnostic of subtypes (Leddy et al., 2015).

Subtypes are not mutually exclusive and there is often overlap with various conditions. Neglecting to assess all subtype impairments may lead to ill-informed decision-making about the state and course of the concussion.

Figure 3b: Subtypes of concussion discussed in this article.

In summary, it can be agreed that concussion is a complicated injury with a clinical minefield of potential symptoms attributable to a multitude of metabolic, neurological, immunological and even gastro-intestinal changes, each taking place in synchrony.

This discussion will now proceed to elaborate on the vestibular, oculomotor, and cervical components of concussion, extending also to some explanation about the function and justification of testing balance (for concussion), and finally, post-concussion exercise rehabilitation.

The characteristic symptoms/subtype classifications of headaches, cognitive and emotional changes, along with sleep disturbances, are all complex and in-depth topics unto themselves, and although all subtypes are sensitive to the same pathophysiological changes, they will remain excluded from this discussion.

Vestibular

The vestibular system is responsible for providing the brain with a sense of motion, head position, and spatial orientation.  It is comprised of a peripheral part, consisting of the inner ear and vestibular portion of cranial nerve VIII, as well as a central part, consisting of nuclei in the brainstem along with a network of connections including those to the eyes, spine, and cortex.

Vestibular dysfunction represents an important subtype of concussion because of its high prevalence and association with prolonged recovery.

When assessing the vestibular system, it is helpful to distinguish between peripheral and central vestibular dysfunction.  Peripheral disorders due to concussion are mainly those associated with dysfunction of the peripheral vestibular apparatus, including the semi-circular canals and otolith organs, located in the inner ear.

With respect to the peripheral vestibular regions it is often the semicircular canals which give a sense of “spinning” whereas damage to the otolith organs are more likely to cause a feeling of unsteadiness and tilting/falling (Akin, Murnane, Hall and Riska, 2017).

A common peripheral disorder is benign paroxysmal position vertigo (BPPV), resulting from dislodged otoconia interrupting normal function of the semicircular canals.  The mechanism of head injury could explain the dislodgement of otoconia which could cause BPPV in the peripheral region.  In one study, looking at the prevalence of vestibular-related symptoms in concussion, BPPV was found in 17% of TBI patients.  Although most recovered with a simple maneuver to reposition the otoconia, the recurrence of BPPV at 6-month follow-up was 40% (Haripriya et al., 2018).

Disruption to the central vestibular region is characterized by symptoms related to movement and the orientation of the body to space and time, such as visual motion sensitivity (VMS).  This category of symptoms includes dysfunction of the vestibulo-ocular reflex (VOR), the vestibulo-spinal reflex (eg. Imbalance), and gait (Lumba-Brown et al., 2019).  In symptomatic, mTBI subjects there is evidence of diffuse axonal injury to the central vestibular system.  Axonal injury has been shown in the cerebellum with an MRI-based neuroimaging procedure called diffuse tensor imaging (DTI) (Akin, Murnane, Hall and Riska, 2017).

Clinically, there may be some overlap of findings, making it difficult to determine exactly what proportion of symptoms are related to peripheral versus central dysfunction.  In general, impairment of the vestibular apparatus, nerves or central vestibular pathways can cause a variety of symptoms such as, but not limited to, blurred vision, complaints of dizziness and imbalance (Akin, Murnane, Hall and Riska, 2017).

Figure 5: Representation of the outer ear (A), middle ear (B) and inner ear (C). (Wallace and Lifshitz, 2016)

The word “dizziness” is often loosely used to describe a variety of symptoms including vertigo (illusion of movement), disequilibrium (unsteadiness) or light-headedness (pre-syncope). It can result from dysfunctional integration of the vestibular and ocular systems, pointing towards the need for a comprehensive assessment of each system to tease out insufficiencies present after concussion (Kontos, Deitrick, Collins and Mucha, 2017).
The dizziness handicap inventory (DHI) is a useful screening tool that is effective in measuring dizziness after concussion. This 25-question inventory assesses the functional, physical, and emotional effects of dizziness.
Because “dizziness” is such a common subjective complaint after head injury it is wise for the specialist assessor to ascertain with careful detail the exact symptoms representing the term. Often it is this detailed explanation which can allude to the region of dysfunction.
It should not be forgotten that dizziness can be related to migraine, cervicogenic, psychiatric, or vestibular dysfunction, however, when it is of a vestibular origin it is then amenable to vestibular and oculomotor rehabilitation strategies (Kontos, Deitrick, Collins and Mucha, 2017).

The bedside tests for vestibular and oculomotor assessments leaves to chance the possibility that subtle yet significant findings are missed. This barrier, along with a relative lack of available technology for more definitive, quantitative testing for oculomotor and vestibular impairments, makes them at risk of being poorly understood or completely overlooked. Unfortunately, involvement of these categories is also likely to result in prolonged recovery when left untreated (Lau et al., 2011).
A relatively new assessment battery called the VOMS (vestibular/oculomotor screening) tool, attempts to give assessors the opportunity to quickly identify vestibular/oculomotor impairment. Five domains are tested whilst symptom provocation is observed and recorded. Tests include smooth pursuit, horizontal and vertical saccades, convergence, horizontal and vertical VOR, and visual motion sensitivity.
Convergence is assessed based on the average measurement of 3 trials of near-point convergence distance, in centimetres.
The VOMS test correlates highly with the Post-Concussion Symptom Scale in determining concussed patients from healthy controls. However, it must be remembered that the VOMS is a screening tool and so only provides a general overview and indication of an impairment that may require more comprehensive assessments to aid in recovery, post-concussion (Kontos, Deitrick, Collins and Mucha, 2017).

Due to the shared circuitry between the central vestibular and visual systems, a comprehensive oculomotor examination can help distinguish central from peripheral vestibular disorders. Unfortunately, this examination is often not performed until the chronic stage (10-12 weeks) of post-concussion despite usefulness in the acute scenario (Wallace and Lifshitz, 2016).

To evaluate the vestibular system a series of tests must be performed. An outline of some recommended tests is listed below:

Vestibular examination:

– Dix hallpike test : to test for BPPV (posterior and anterior canals)
– Roll test : to test for BPPV (horizontal canals)
– Headshake test: to test for unilateral vestibular hypofunction
– Vibration test: to test for unilateral vestibular hypofunction
– Head impulse test: to test for overt or covert saccades in response to impaired VOR
– Dynamic visual acuity test: a VOR test for decreased visual acuity during head movement

Oculomotor examination:

– Vertical and horizontal saccades
– Vertical and horizontal pursuits
– Fixation
– Convergence
– Visual VOR / VOR suppressed
– Vision-denied gaze assessment
– Skew test
– Saccadometry

Therapy for vestibular disorders depends on the type of dysfunction. BPPV can be treated with canal repositioning manoeuvres whereas VOR impairments can be improved by gaze-stability exercises which include head-eye coordinated movements with the goal of keeping the gaze fixated on a target.

Visual motion sensitivity can be improved by a graded exposure to visually “challenging” environments which are likely to provoke symptoms and force habituation to the visual stimulus, thereby desensitizing the subject’s symptoms. Improvement of balance is achieved with compensation to activities which challenge balance, such as dual-tasking, sensory-organisation training and dynamic balance training (Wallace and Lifshitz, 2016).

Interestingly, cognitive impairments have been noted to improve after subjects with PCS have undergone vestibular therapy, illustrating evidence of the neurological link between vestibular and cognitive regions of the brain (Alsalaheen et al., 2010).

Oculomotor

The oculomotor system uses both voluntary and involuntary movements to enable the tracking and fixation of a target-of-interest onto the fovea – an area of the retina which is important for visual acuity.

The clarity of an image declines by as much as 50% if the target moves only 2 degrees from the centre of the fovea. Since there are two eyes, the brains’ goal is to accurately and synchronously engage the 12 eye muscles to move each eye into a position so that the target image is on the fovea, within 0.5 degrees, giving clarity and correct depth perception (Leigh and Zee, 1999).

This intricate and fine-tuned process has much room for error which gives rise to the many findings of dysfunction in the oculomotor system.

Vision and the various types of eye movements have collectively have been shown to activate over 50% of the brain, making a diffuse brain injury very likely to affect the broad networks responsible for the visual system (Debacker et al., 2018).

Various eye movement types have distinguishable characteristics, such as speed and direction, each engaging specific neurological pathways. This makes oculomotor assessments a practical and sensitive measure of brain function and recovery after concussion and other forms of traumatic brain injury (Ventura, Balcer, Galetta and Rucker, 2016). A meta-analysis of 181 papers between 1960 to 2016 showed that oculomotor deficits following TBI were long-standing and therefore concluded that because oculomotor tests reflect neural integrity they may provide a “sensitive and objective biomarker” for brain injury (Mani, Asper and Khuu, 2018).

Figure 6: The complex network of integrating cortical and subcortical structures involved with eye movement. (Ventura, Balcer, Galetta and Rucker, 2016)

In May, 2019, the Australian Journal of General Practice conducted a review of papers over the last 10 years which included research on oculomotor dysfunction following concussion.

The table below, taken from the review, is a list of symptoms and signs which appear consistent with mTBI.

Table 2: Symptoms and signs affecting the visual system following a concussion

(RACGP – Persistent visual disturbances after concussion, 2020).

Visual disturbances have been well documented as a common complaint of concussion, with subjective reports of blurriness, double-vision, decreased attention and eye-fatigue. There have been reports to demonstrate all types of eye movement disturbances following concussion, including that of saccadic eye movements, smooth pursuits, accommodation and vergence.  Prevalence rates for such disturbances following mTBI may be as high as 69% (RACGP – Persistent visual disturbances after concussion, 2020).

Like the vestibular system, it has also been shown that poor oculomotor function correlated with a higher level of post-concussive symptoms, as well as poor function in activities of daily living (Heitger et al., 2009).  As aforementioned, the oculomotor system shares much of the same circuitry as the vestibular system, therefore making them intricately linked and prone to a cross-over of reported symptoms, as well as serving as a mechanism of distinguishing between peripheral vestibular and central vestibular involvement.

Listed below are further studies which give evidence of oculomotor impairments noticeable after brain injury:

1.  Ventura et al states that acute mTBI patients were found to have “impairments in memory-guided saccades and anti-saccades, with increased latencies, higher directional errors, and poorer spatial accuracy”. The author’s opinion is that much promise lies in using video-oculography to assess the quantitative changes in pursuits and saccades (Ventura, Balcer, Galetta and Rucker, 2016).
2. Compared to control subjects mTBI patients demonstrated impairments in predictive smooth pursuit eye movements. This study, carried out in 2006, goes on to suggest that the decreased target prediction of smooth pursuits, which requires a certain amount of cortical function, correlates to the cognitive deficits of the concussed subject (Suh et al., 2006).
3. In 2016, concussed patients were compared to non-concussed patients and it was found that the concussed patients had prolonged inter-saccadic intervals and larger deviations of saccade endpoints, as measured on infrared-based video-oculography (Rizzo et al., 2016).
4. A study of 100 concussed adolescents (aged 11-17 years), released in 2016, found that 51% had accommodative disorders, 49% had convergence insufficiency and 29% had saccadic dysfunction. Overall, 46% of subjects had more than one vision disturbance (Master et al., 2015).
5. In a study of 92 subjects with TBI, vertical smooth pursuits analysis could distinguish between severe and moderate TBI sufferers, but not between mTBI and non-concussed subjects (Hunfalvay et al., 2020).
6. 64 patients, seen approximately 5-10 days’ post-concussion, were compared with 78 controls. Eye movement tests (smooth pursuits, vertical/horizontal saccades, convergence) provoked symptoms in 33-42% of patients. Additionally, near point convergence measures were 4.0cm greater in concussed patients (Mucha et al., 2014).
7. A study in 2019 shows that using eye-tracking technology to measure self-paced horizontal and vertical saccades is a reliable and objective method of identifying subjects with varying severities of TBI (Hunfalvay et al., 2019).
8. In a group of 36 PCS subjects compared to 36 non-PCS subjects is was found that the PCS group executed a smaller number of self-paced saccades, with longer inter-saccadic intervals, as well as slower velocities and longer saccade durations. There was also found to be a greater number of errors during anti-saccades, implying not only the sub-cortical regions, but cortical regions of the brain and the connections in between. Furthermore, cognitive functions likely to be affected in the PCS group, based on dysfunctions of the oculomotor tests, include things such as response inhibition, decision making, short term spatial memory and visual attention (Heitger et al., 2009).
9. In 2016, an analysis of 218 concussion cases for subjects with vision problems concluded a high prevalence of convergence insufficiency and accommodation insufficiency, both of which showed improved outcomes with vision therapy (Gallaway, Scheiman and Mitchell, 2017).

Due to the varying measurement methods and metrics used in research, there is still some inconsistencies in the evidence around oculomotor examinations for concussions.  However, there is mounting evidence in the literature towards eye-tracking as a useful tool for concussion.  Many saccadic and pursuit deficits, however, may be missed with the naked eye upon clinical examination, therefore eye-tracking technology may be a useful tool for sensitive monitoring and screening for sports-related concussion (Snegireva, Derman, Patricios and Welman, 2018).

Future research is likely to clarify some of the questions around the most effective tools and processes for eye-tracking as a measure of concussion.

Even though surgical or medical intervention may be indicated for rare cases such as muscle paralysis or nerve palsies, it is well recognized that vision therapy is an effective intervention for oculomotor impairments (Kapoor and Ciuffreda, 2002).  Two random controlled trials for conservative management for convergence insufficiency and accommodative insufficiency concluded that vision therapy was effective in children for managing both conditions (Broglio et al., 2015).

To obtain some guidelines on the best practice, some research has been devoted to the question of oculomotor therapy (OMT), and more specifically, durations and frequencies of interventions.  In one study for oculomotor training for reading, post brain injury, it was recommended that twice per week for 8 weeks would improve pursuits, saccades, and fixation, and improve multiple line reading (Ciuffreda, Han, Kapoor and Ficarra, 2006).

Another study recommended 36min of training in 60min (24min being rest) twice per week for 11 weeks, and yet another study recommended OMT at a ratio of 15min training per 5 min rest for a total of 9 hours over 6 weeks (Thiagarajan and Ciuffreda, 2014).

It is unlikely that there is a perfect training regime for oculomotor therapy due to the heterogeneous nature of eye-movement impairments.  It is recommended that therapy be devised on a case-by-case basis, with subjective reports of symptom provocation guiding the clinician’s choice of graduated exposure to eye movement and processing “loads”.  There should be a view towards neuroplasticity and adaptation of the brain over a duration between 2 weeks to 6 months.

Cervical

Although it is proposed that neck-related symptoms can contribute to the persistent symptoms of post-concussion syndrome (Kennedy, Quinn, Chapple and Tumilty, 2019) there is generally little evidence of the association between cervicogenic impairment and mTBI, and hence a poor understanding of the connections and similarities between the two  (Morin, Langevin and Fait, 2016).

Symptoms of dizziness, neck pain, and headaches can be overlapping in both concussion and whiplash, making it somewhat hard to differentially diagnose.  However, the mechanisms thought to provoke these similar symptoms, are different – the concussion mechanism is thought to be from metabolic and mechanical injury to neurons and peripheral organs, whereas the cervical mechanisms are thought to arise from damage to the proprioceptive inputs involved with head and neck position sense.

Afferent inputs from the cervical spine are integrated with visual and vestibular inputs in the cerebellum via the spinocerebellar tract, as well as converging directly onto the vestibular nuclei and superior colliculus.  These networked inputs allow for adaptive regulation to both the oculomotor and postural efferent pathways, which enables gaze stability, postural control and balance.  It is thought that aberrant afferent inputs of C1-3 can create a sensory mismatch when converging with normal inputs from the vestibular and visual system, causing the cervicogenic symptoms of dizziness, headaches or vertigo (Cheever, Kawata, Tierney and Galgon, 2016).

Figure 7: Major structures related to cervicogenic symptoms and concussion

(Cheever, Kawata, Tierney and Galgon, 2016).

In 2019, a review of cervical injury following concussion reported that there was a high prevalence (90%) of impairment with respect to muscle tension, joint mobility, and muscle strength.  The study used the neck disability index (NDI) as a standardized self-scoring guideline to indicate the severity of the neck disability. From this study, it was recommended that there be a framework in place which gives specific attention to the needs for testing for these impairments, such as ligament laxity tests and muscle endurance tests (Tiwari et al., 2019).

Diagnosing cervicogenic involvement requires assessment of the cervical afferents whilst minimizing visual and vestibular input, to observe any disruption of oculomotor and balance functions.  Two recommended tests are the “joint position error test” and the “smooth pursuit neck torsion test”.

It is also recommended to test for symptom provocation and laxity in the alar (rotational/lateral movement between head and C2) and transverse (anterior glide of head from C2) ligaments, as well as consider the endurance of the neck flexors with tests such as the “neck flexor endurance test”.  Observation should also be made with regards to general posture, upper-limb biomechanics, and overall laxity of the subjects’ ligaments in the body (Tiwari et al., 2019).

It is known that children have a decreased muscle bulk around the neck and have proportionally heavier heads, which gives logic to the notion that children are less able to control the concussive forces to the head, and are therefore more likely to suffer associated cervical impairments.  A study of 6704 high-school athletes found a relationship between concussion and neck-strength, neck circumference and head-to-neck ratio, whereby those with weaker, thinner necks, were more likely to be concussed.  It was postulated that athletes with these characteristics are targeted for preventative measures to improve neck strength (Collins et al., 2014).

In addition to this, another study of 3832 male ice-hockey players found that the baseline characteristics of “headaches” and “neck pain” were risk factors for concussion.  This gives further insight into potential pre-screening requirements for preventative measures (Schneider et al., 2013).

In 2014, a randomised controlled trial of 31 subjects with persistent symptoms of neck pain, headache or dizziness, were given general rest followed by graded exertion, range of motion exercises and postural advice. 73% of the treatment group, who received additional cervical and vestibular rehabilitation, were found to return to participation in sport within 8 weeks, compared with only 7% of the control group (Schneider et al., 2014).

It is critical to remember that there are overlapping symptoms between concussion and cervicogenic injuries.  An understanding of the mechanisms of each injury, along with differentiating assessments, may help distinguish between the two presentations and lead to important differences in treatment techniques.

Balance

Although balance is not included as a specific subtype category of concussion, it is well recognized as a potential functional impairment of the injury, and hence is worthy of measurement.

The function of balance is an output of three sensory inputs – the visual, vestibular, and somatosensory senses.  Because of this network of contributing factors, balance alone is a non-specific indication of neurological deficit.  All inputs integrate into the central nervous system whereby they are processed to produce both static and dynamic balance control.  Decreased balance can represent impairments in the vestibular system, visual or somatosensory system, or in the central integration of all three systems (Fino et al., 2017).

Figure 8: Sensory systems contributing to static and dynamic balance (Fino et al., 2017).

The Rhomberg test, with eyes closed and feet together, has traditionally been used as an assessment of balance in the “falls-risk” subject but it does not adequately challenge the typical concussed athlete.  The current standard in balance for the concussed subject is the balance error scoring system (BESS).  It is a cost-effective and easy balance assessment included in the SCAT5 assessment battery for monitoring balance performance.  However, the BESS has been criticized for having low sensitivity for the high-level athlete because it is not challenging enough. Additionally, postural control in most concussed athletes will return to normal within 3-5 days, making balance unreliable as a stand-alone diagnostic or measuring tool (Ruhe, Fejer, Gänsslen and Klein, 2014).

Instrumented force plates, which are becoming more cost-effective and portable, now offer a practical way of obtaining quantifiable measurements of postural sway.  Using force-plate technology offers more sensitivity to static tests such as the BESS assessment.  Another static test is the “clinical test of sensory organisation and balance” (CTSIB) which measures balance under various conditions that challenge vision and vestibular inputs.  It is recommended that dynamic balance also be included in the assessment of balance for the concussed athlete, due to the higher level of balance-performance required in sports (Johnston, Coughlan and Caulfield, 2016).

Two of the main neural networks of the vestibular system include that of the vestibular-ocular system and the vestibulo-spinal system.  The vestibulo-ocular system is concerned with gaze stability and therefore impairments in this region may present as blurred vision, dizziness, and visual instability.  The vestibulo-spinal system represents a different pathway that is concerned with balance.  Because these two pathways are not identical, impairments in each system is not mutually inclusive (Mucha et al., 2014).

In a study in 2014, further investigations were made into the links between balance and the vestibular system and oculomotor control.  This study tested post-concussive subjects with normal subjects and showed that concussed subjects were more likely to deviate their gaze from a centre target whilst performing task-related movements of the body in response to visual information.  The interpretation of the results explained that the disrupted vestibular integration of the post-concussive subjects would lead to over-corrective or under-corrective eye movements in response to improper head movement responses whilst balancing (Murray et al., 2014).  Essentially, this study showed that the visual system of the concussed subject will compensate to account for the impaired vestibular system.

In summary, balance cannot alone be related to any specific disorder of the brain due to its multi-modal function.   For example, “dizzy” patients with balance disorders are not necessarily related to vestibular dysfunction.  Balance can, however, be a useful adjunctive measurement to assess overall function and is an important inclusion in rehabilitation for safety and performance purposes.

Return to exercise / return to play

Considering many concussions are received during sporting seasons, a very important question to answer is “when is it safe to return to play?”.

In 2014, a retrospective study of 170 charts of concussed high-school and college athletes were reviewed over a 5-year period.  The study found that in 43.5% of cases, the athlete returned to sport too soon.  It was also found that subjects with a previous history of concussion were more likely to need longer periods of rest before initiating physical activity after injury (Carson et al., 2014).

In the past two decades, the management of concussion has changed and has done so with a reduced risk for repeated injury during the critical period of vulnerability.  The average return to play period in 1999-2001 was 3 days, however, it was found that the risk for re-concussion within the 10-day period was 92%.  In 2014-2017 a new approach was taken whereby the concussed athlete avoided competition until symptom-free.  It was found that the average return-to-play period, governed by this waiting period, was 12 days, resulting in a 3.7% risk of re-concussion within 10 days (McCrea et al., 2019).

This tendency towards an extended waiting period supports the general international guidelines which emphasise a longer duration for brain repair than previous years.  The significant change over the years could reflect the gain in information with advances in technology and further research into the delicate balance required for proper neuronal function.

In 2013, researchers did an investigation into the sub-concussive head impact of soccer players.  This study used diffuse tensor imaging to show that there was an association between the number of “headers” and axonal injury in a specific area, concluding that accumulative brain damage could be occurring even without a history of concussion (Lipton et al., 2013).

Although there have been mixed reports about whether repetitive sub-concussive head impact causes any detrimental effects to the brain, most findings support an unfavourable outcome, with evidence on imaging mounting towards changes in brain white matter and, most commonly, impairments in neurocognitive functions of memory and processing speed (Sports-Related Concussions in Youth: Improving the Science, Changing the Culture, 2015).

A more recent study in 2020 has taken technology and research one step further by showing that the impairments of repetitive, sub-concussive impact in 24 female soccer players were more apparent via EEG recordings of the brain whilst performing a continuous performance task during moderate exercise, as opposed to at rest.  The findings of this study may serve as a guideline for testing and treatment protocols (Harriss et al., 2020).

There is much to consider when deciding when it is best to abstain from physical and cognitive exertion, when to gently return to activity at any level, and then when to return to competition.

One theory towards the need for rest for recovery is that the high glucose demands of the injured brain are impeded by increased activity levels, and therefore can impair the needs of the healing brain.  Another more obvious reason for rest is to avoid secondary injury and the possibility of the catastrophic “second impact syndrome”, whereby the damage of the injured brain is catalysed by further insult within a time when is it metabolically very susceptible (Broglio et al., 2015).

Many acute symptoms of concussion will abate within 24-48 hours, with complete resolution of the injury being no longer than 10-14 days.  However, the definition of resolution seems to be an area that is unclear.  There is a wide variation of statistics around just what proportion of concussions extend beyond 14 days and it is not unusual for concussion symptoms to be ongoing at 5-6 weeks post-injury.

According to a study by Leddy et al, 2010, concussed subjects with prolonged symptoms (up to 5-6 weeks) are more likely to decrease symptoms and return to sport when undergoing a careful and moderate exercise routine.  The return to exercise is best to be measured specifically via subjective reports on symptom provocation.  This should be coupled with a graduated, adaptive increase in intensity (Leddy et al., 2010).

The CISG recommends a 6-stage return-to-sport which starts by limiting all activities that provoke symptoms.  The steps in the activity phases then progress as follows:

– light aerobic activity (without shortness of breath and avoid resistance training) until symptom-free,

– then progressing to sport-specific drills which are non-contact and with no head impact,

– progressing to more complex sport-specific drills, still without contact (may add resistance training),

– and then to full-contact practice following medical review,

– and finally normal competitive sporting activity.

A minimum of 24 hours should be spent at each level before progressing to the next level, and any recurrence of symptoms indicates the need to step-down to the previous level (McCrory et al., 2017).

For a more detailed guideline to returning to activity, Leddy et. al, 2013, have created the Buffalo concussion treadmill test (BCTT).  This test serves as a protocol for exercise tolerance and can be used to evaluate the physiological limitations for exercise, post-concussion.

The BCTT determines exercise capacity by gently increasing the heart rate of the concussed person, whilst monitoring symptoms along the way.  The test results will indicate the most appropriate heart-rate threshold (HRt) at which the person should exercise, as well as give some indication into the need for further investigations into vestibular and cervicogenic impairments.

It is recommended that the exercise dosage is 20min/day at 80% of HRt, for 2 weeks.  Then, if tolerated, exercise intensity can be increased to 85-90% of HRt over the next 2 weeks. Once this exercise intensity has been achieved without consequence the subject may begin a graduated return-to-play (Leddy and Willer, 2013).

It should be noted that cognitive and emotional categories are not evaluated during the BCTT, however, there is consideration for vestibular-ocular and cervicogenic contributions to post-concussive symptoms.   Further studies have tested the reliability of the test when using an exercise bike instead of a treadmill and it was concluded in 2019 that both tests are equivalent (Haider et al., 2019).

One difference when using the treadmill versus the bike is that walking on a treadmill results in many more movements of the head.   There may be more provocation of vestibular-related symptoms on the treadmill test due to the influence of head motion on the vestibular system and integrated vestibulo-spinal and vestibulo-ocular pathways.

A 2019 review of the literature found a moderate amount of evidence to support aerobic exercise as a treatment for post-concussion syndrome.  A 6-week timeline of exercising at 80% of the symptom threshold is recommended, however, this timeline has not been validated.  It was noted that athletes, compared with non-athletes, responded faster to the exercise as a treatment for post-concussion syndrome (Ritter, Hussey and Valovich McLeod, 2019).

Figure 9: Exercise tolerance protocol and suggested diagnostic guidelines (Leddy and Willer, 2013).

Conclusion

There has been much research over the past twenty years dedicated to understanding the complexities of concussion.  In recent years, it has been suggested that concussed persons recover within 7-14 days, however, some people will have prolonged recoveries lasting from months to years.  A concussion injury can be diffuse, with complex pathophysiological changes, and therefore can present with a large variety of symptoms, incorporating many regions of the brain.  For effective assessment and management of concussion, it is beneficial to understand the various subtypes of concussion.  Both vestibular and oculomotor subtypes have been discussed in this article and there is evidence that these categories are associated with prolonged recovery, especially when left untreated.

It is also possible that a head injury could cause damage to the cervical spine, resulting in symptoms which can overlap with concussion, yet requiring distinctly different treatment strategies.  Specific testing of the cervical spine should be considered for all head injury patients.

Balance is useful as a measure of overall function of the integration of visual, vestibular and somatosensory systems.  Balance assessments should provide an appropriate challenge to the subject in accordance with their functional capacity and should include dynamic balance testing.  Finally, the evolution of return-to-play criteria has been explained as it has evolved over the past two decades.  Returning to exercise and sport should be guided by an exercise tolerance assessment and it may be that athletes will return quicker when exercising during rehabilitation at a moderate aerobic capacity.

In summary, a preliminary assessment of concussion ought to identify regions of interest in the acute stage of the injury, followed with a thorough examination of each category, preferably using quantitative measurement tools.  For clinically better outcomes, evidence-based interventions should then be strategically applied, based on detailed assessment findings and reviews.

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