Concussion Rehabilitation

Abstract

Concussion represents one of modern medicine’s biggest challenges. As we are gaining more and more information on pathophysiology, diagnosis, and treatment, a lot is still to be cleared. On the side of pharmacology, rehabilitation is the leading treatment for concussion signs and symptoms. From acute to the chronic phase of brain dysfunction, rehabilitation is nowadays providing help to people recover faster and better. In this chapter, we will analyze in depth the key information and evidence supporting current concussion rehabilitation methods and protocols. Through this chapter, we are exploring how aerobic training, vestibular rehabilitation, and oculomotor exercises are working together with the treatment of migraine and neck pain. We also aim to provide the basis and relevance of cognitive rehabilitation and double-task-multifunctional training and the importance of fatigue and mood problem management.

1. Introduction

A concussion is a mild traumatic brain injury caused by a direct blow to the head, neck, or elsewhere in the body, resulting in an impulsive force being transmitted to the brain. This initiates a neurotransmitter and metabolic cascade, with possible axonal injury, blood flow change, and inflammation affecting the brain [1]. This leads to a brain functional impairment that provokes signs and symptoms, such as headache, neck pain, nausea, balance problems, gait impairment, dizziness, fatigue, sleep disturbances, mood changes, cognitive and focus impairment, less tolerance to cognitive and physical exercise, blurred vision, and visual problems. This is a reversible condition that usually resolves within 2 to 4 weeks, but it can last months or longer [2, 3]. Experiments on rats demonstrate that, during this period of time, brain cells undergo an energy crisis and are more vulnerable to new traumas because of blood flow changes [4, 5, 6, 7]. Advanced neuroimaging studies on humans seem to validate these findings [3]. During brain vulnerability period, any additional concussions can lead to an acute more aggressive brain injury, known as diffuse cerebral swelling, or to a progressive subclinical injury summation until massive cell death and encephalopathy, best known as chronic traumatic encephalopathy [8]. United States Centers for Disease Control and Prevention (CDC) have labeled concussion a major public health issue due to acute and potential long-term effects associated with this injury [9]. Nowadays, many concussions still remain undiagnosed, and above all sport-related concussions [10], but the trend is positive. Over the past decade, knowledge about concussion has increased significantly, with increasing hospital consultations [11] and medical attention.

On actual knowledge, avoiding second-impact exposure and treating concussion with clinical and objective recovery are the key in preventing brain traumatic encephalopathy. That is why it is so important to know how to manage and treat concussions.

2. How concussion evaluation is important for rehabilitation

A concussion is a complex heterogeneous injury that presents with a variety of symptoms and clinical findings. The primary goal in concussion evaluation is to characterize the clinical presentation, identify factors of possible prolonged recovery and prescribe a specific treatment plan.

Clinical presentation is different in every concussion by symptom types, intensity, and duration. Researchers have attempted to classify concussions into specific clinical profiles, to help clinicians with prescription and follow-up. Clinical profiles are supported by intuitive evidence, but to date, they are not empirically validated. Nevertheless, they are useful for educational purposes and help in clustering and focusing on current concussion rehabilitation indications. Moreover, it can help in drawing a tailored rehabilitation protocol, which seems promising in concussion recovery, instead of a one-size fits all approach.

Here, we report the main clinical profile classification proposed by the literature.

Collins et al. [12] categorized concussion into five clinical profiles and two modifying factors. It is based on symptoms evaluation and physical examination only; it can be applied from the first week following injury and profiles are not mutually exclusive as the overlap is possible:

1. Vestibular

2. Ocular-motor

3. Cognitive/fatigue

4. Post-traumatic migraine

5. Anxiety/mood

Modifying factors are:

1. Cervical

2. Sleep disturbances

Ellis et al. [13] proposed a classification into three post-concussion disorders and two modifying factors, which can be applied after 3 weeks from injury and it is based on symptoms evaluation, physical examination, and aerobic treadmill testing.

1. Physiological

2. Vestibular-ocular

3. Cervicogenic

Modifying factors are:

1. Mood disorders

2. Migraine

In other studies, even if a classification is not proposed, researchers identify the necessity to have a targeted evaluation and rehabilitation protocols for symptoms, such as headache, insomnia, cognition, mood, balance, vision, and fatigue, if symptoms last more than a month, which recall symptoms identified in the previous classifications.

Clustering patients’ symptoms into this clinical profile are helpful for tailored treatment prescription, which we will describe soon in this chapter. A recent review states that individually tailored multimodal interventions have a worthwhile effect in providing a faster return to sport and clinical improvement, specifically in those with persistent symptoms [9, 14, 15]. Collecting a good clinical history is also fundamental. Identification of existing pre-injuries factors that can influence recovery is mandatory.

It has been demonstrated that the natural history of concussion, from 70% up to 85% of cases, is a spontaneous recovery within 2 weeks for adults and 4 weeks for children and adolescents. Patients will experiment with a natural reduction in symptoms by number and gravity through days, without any particular intervention [16, 17]. This means that, after diagnosing a concussion, an observational approach could be part of the treatment process, as Nature is working on its own to promote spontaneous recovery. Nevertheless, it is crucial to know that symptoms and clinical recovery could happen in a shorter time than brain complete function recovery. Preliminary studies have shown that brain normal functioning recovery could last longer than the symptoms perceived [3, 18].

Moreover, we should remember that 15–30% of concussions are going to have a prolonged recovery, and they will need a different approach and treatment. Thus, it is really important for a clinician, to draw up a precise clinical history to help understand if a wait-and-see approach is actionable, or close surveillance and a more active treatment is necessary.

Prolonged post-concussion symptoms (PPCS) and post-concussion syndrome (PCS) are labels used to identify symptoms lasting more than 4 weeks. Researchers are trying to understand recovery trajectories and predict prolonged recovery time as a way to stratify patients for a tailored rehabilitation and treatment protocol.

Nowadays, there are no objective measures to predict prolonged recovery: salivary biomarkers and advanced MRI spectroscopic imaging are promising fields of research, but more studies need to be done before application in clinical settings [3, 19]. Nevertheless, some factors on clinical presentation and history seem, on actual knowledge, to predict recovery time.

Symptoms severity score and overall symptom burden seem to be the most significant predictor of prolonged recovery [10, 20, 21, 22], history of previous concussions, sleep disturbances [23], vision and vestibular problem and a history of motion sickness seems to predict prolonged recovery in children [24], prior diagnosis of mental health problem, as depression, anxiety, bipolar and personality disorder are predictive for prolonged recovery [25], prolonged rest and delay in search for medical attention relate to a longer recovery time too [26].

Physical examination and objective tests are also important to determine a patient’s actual impairments and to discover new emerging factors that could predict a longer recovery. For example, cognitive impairment, such as reaction time and visual motor speed performance in neurocognitive testing, relates to prolonged recovery [20, 27].

Once collected all the information, clinicians are ready to give treatment indications and prescribe rehabilitation.

Part of concussion treatment is based on medication, but it will not be discussed, as it goes beyond the aim of this chapter.

3. Treatment indication and tailored rehabilitation

3.1 Do not harm: avoiding a second impact

First do not harm, state the Hippocratic Oath. Protecting a patient from a second brain impact, especially if close to the one he/she is suffering, is mandatory. As said before after a brain injury, even if mild, the brain lays in a state of vulnerability [1], and a second impact could lead to a Second Impact Syndrome (SIS) or diffuse cerebral edema, with the greatest risk occurring in the first 10 days post-injury [16]. It is particularly true in sport-related concussion because of possible repetitive traumatic events [28], related to sports characteristics. Returning an athlete to play with persistent symptoms may predispose the athlete to a higher risk of a new brain impact injury as concussion decreases the cognitive ability and reaction time, which theoretically diminished an athlete’s ability to respond to the demands of the sport. Attention should be paid also to other environments, thus reducing risk exposure to driving, home accidents, or work accidents is recommended until medical clearance.

3.2 Observation as the first step of concussion treatment

If clinical history and physical examination are not suggestive of prolonged recovery, an observational approach could be part of the treatment process, as Nature is working on its own to promote spontaneous recovery. As said before, 70–85% of concussions will recover spontaneously, and follow-up could be a good managing decision. Nevertheless, we should also remember that medicine is not an exact science, so follow-up is always recommended.

Usually, behavioral modifications are suggested:

• Regular schedule of sleep and meals.

• Good hydration.

• Do not take drugs or alcohol.

• Do not take medicine if not prescribed.

• If symptoms worsen, go to seek medical attention.

If the clinician is an expert in managing concussion, an active and individualized approach is always recommended, but if patient history and symptoms do not depict a serious clinical presentation, remember that sometimes wrong prescriptions are worse than no prescription.

3.3 Rest: is it useful in concussion treatment?

During the acute post-injury period, patients who suffered from concussion usually experience intense symptoms that are worsened by cognitive or physical activity, and assuming that vigorous activity could magnify the underlying energy crisis is reasonable [9, 29, 30]. Moreover, as said before, a second impact during the period of brain vulnerability could lead to more aggressive injury and CTE [31, 32, 33, 34]. Literature also demonstrates that delayed reporting and removal from athletic activity following a sports concussion, predicts prolonged recovery [35], meaning that early physical activity could relate to a longer recovery period. These are the main reasons why most clinicians prescribe rest until symptoms improve, and in the previous decade, rest was highly recommended [9].

Nevertheless, it is important to notice that avoiding contact during this period and rest are two different strategies. If the first one is always recommended as far as the patient remains symptomatic or until medical clearance, the second one is open to different management.

Researchers noted that patients with the highest and lowest levels of activity had worse outcomes and took longer to recover, suggesting that too much or too little physical and cognitive activity could be detrimental to recovery [31].

Strict and prolonged rest in medicine is demonstrated to be of no benefit. It exacerbates symptoms and prolongs recovery [36], and the same thing applies to brain injury [37].

In addition, we should also state that strict rest, meaning no physical or cognitive activity during the time prescribed, forces people who suffer from concussion to avoid sports, social life, and school or work. This has a big impact both on the patient’s psychology and on the society [9].

In contrast, there is increasing evidence that early mild noncontact, such as physical activity, does not appear to worsen or cause additional injury and indeed seems to help recovery [9, 17, 37, 38].

So, how is rest beneficial? How much and how long should rest be prescribed?

Evidence from the last 10 years showed that strict rest beyond 2 days will prolong recovery from concussion [37, 39, 40, 41], and that symptoms are of greater magnitude.

In agreement with that, the concussion consensus in the sports group set an average rest period of 24–48 hours after a concussion trauma, before starting rehabilitation and progressive return to physical and cognitive activity [2]. During the first few days, rest should not be strict avoidance of physical and cognitive activity [31], but should be dosed, based on the patient’s sensitivity to symptom exacerbation. Physical and cognitive activities of daily living are permitted if they do not exacerbate symptoms, absence from school or work is recommended. A patient could sleep and take naps if needed.

3.4 Physical activity as a medicine for concussion

Many studies demonstrate that physical activity is the principal intervention in concussion management as it helps in recovering faster and lowering symptoms intensity [26]. Thus, it is indicated in any concussion case, even if prolonged recovery is not suspected.

If we consider “physical activity” as a medicine, it is important to understand what is the “active ingredient” and how to dose it. “Physical activity” may include aerobic exercise, resistance training, full body exercise, sport-specific exercise, balance and vestibular exercise, visual ocular-motor exercise, postural exercise, multitasking exercise…and so on.

What is known nowadays is that aerobic exercise and full body exercise, in general, are good interventions for concussion recovery, a sort of “one size fits all” approach, while other types of physical exercise are more specific for concussion clinical subtype profiles. So, in this chapter “physical activity” will be synonymous with “aerobic exercise, resistance training, full body exercise, and sport-specific exercise,” while vestibular rehabilitation, balance exercise, motor-ocular exercise, visual rehabilitation, and cervical rehabilitation will be deeply investigated later in this chapter.

It is well established that concussion leads to an altered ionic and cellular homeostasis, that requires more ATP usage to restore the physiological environment. This energy requirement crashes with a setting of reduced cerebral blood flow, resulting in a mismatch between energy supply and demand [32]. The autonomic nervous system is also altered in the concussed patient, and this condition leads to an altered modulation of cardiac function and cerebral perfusion [42, 43].

Introducing aerobic exercise in this setting of the energy crisis is not so straightforward, but at the same time it is well-known that aerobic training could help in autonomic dysfunction recovery [44].

As said before, an average rest period of 24–48 hours after a concussion is recommended, then an initial light aerobic exercise could be initiated, even if symptomatic. The main warning lights that we have in a concussed patient are symptoms. Thus, it is mandatory to count on personal patients’ symptoms and feelings and it is important to establish good cooperation with the patient. The active training could be done independently, but it is recommended to be followed by a personal trainer or physiotherapist, who is trained in concussion rehabilitation.

Based on literature findings, here we provide guidance on validated physical exercises for concussion.

3.4.1 The graduated return to play protocol (GRTP)

The fifth consensus statement on concussion in sports creates an easy graduated protocol to return to sport participation [2]. It is based on the progressive introduction of aerobic and resistance training, mixed with sport-specific exercises. For contact sports, returning to full contact practice is permitted after medical clearance. This approach could be applied to any sport.

The characteristics of this approach are based on progressive physical stimulation and evaluation of symptom exacerbation. Every step should last at least 24 hours and if symptoms worsen with the exercise, the athlete should go back to the previous step.

3.4.2 GRTP

• Stage 1. Symptoms-limited activity: Daily activities that do not provoke symptoms and gradual reintroduction of work/school activity.

• Stage 2. Light aerobic exercise: Walking or stationary bike increases heart rate.

• Stage 3. Sport-specific exercise: running or skating drills.

• Stage 4. Harder noncontact training drills, start a progressive resistance training.

• Stage 5. Full contact practice (following medical clearance): Participation in normal training activities.

• Stage 6. Return to sport: Normal gameplay.

Dosing exercise based on symptoms provocation only is a useful method if no assessment tools are disposable. It can be applied to everyone, athletes or not, helping them to increase physical activity. The graduated return to play protocol is obviously particularly indicated for sports concussion, but the underlying symptoms-based approach could be applied also for people who are not athletes, as a “sub-symptoms threshold method” (see below).

For example, we can use the same protocol by using only aerobic exercises, such as walking, running, and cycling. Every step should last at least 24 hours and exercises should be done on a daily basis or 6 days/week and stay at a sub-symptoms’ threshold level. On a scale from 0 to10, any new symptoms or symptoms worsening of 3 points out of 10 is considered an “exercise symptoms provocation,” and the patient should set his exercise to a lower level, or stop.

The patient should start at a light perceived level of exercise and monitor his symptoms. If no symptoms are provoked, the patient can increase activity level by duration and/or intensity or exercise type and, again, monitor his symptoms. If the exercise provokes symptoms, the patient should set the training at a previous level of exercise for the next 24 hours.

The same pattern could be applied to resistance training.

3.4.3 The concussion sub-symptoms threshold approach

This method is based on the physical activity below the symptoms threshold, which is similar to the previous approach. Nevertheless, it is based on aerobic exercises and a more objective setting and progression.

An initial test should be done to evaluate patient tolerance to aerobic exercise, which has been demonstrated to be lower in concussed patients because of the autonomic dysregulations mentioned before. It is important to set each patient’s threshold for symptom exacerbation because the following physical activity is set on a sub-threshold level, and then a new test for progression will follow.

The most popular and validated test is the Buffalo Concussion test. It is done on a treadmill (BCTT) [45] with a progressive increase of aerobic loading, measuring heart rate and symptom exacerbation. In particular, the patient is asked to wear a heart rate monitor and to step on a treadmill. To increase heart rate, the treadmill is tilted progressively, similar to the Balke treadmill test, until aerobic intolerance. The aerobic threshold is set if the maximum heart rate is reached or new symptoms appear or symptoms are worsened by 3 points on a scale out of 10. The patient is then instructed to perform aerobic exercise at 80% of the heart rate threshold for 20 minutes on a daily basis. If the patient is an athlete, it is recommended to exercise at 90% of the heart rate threshold for 20 minutes twice a day. If patients feel symptomatic while exercising at home, they have to stop and rest and continue the next day at a lower exercise intensity. If not, patients may extend the duration of exercise from 20 to 30 minutes or more, keeping the heart rate steady. A daily symptom diary is recommended to track symptoms exacerbation and exercise progression.

After 1 week a patient could increase heart rate exercise by 5–10% or, if possible, the Buffalo Concussion test should be repeated to set a new symptoms threshold [46, 47].

The test could be performed also on a stationary bike (BCBT) [45].

During the last years, aerobic exercise prescriptions were made easier even in case of a lack of aerobic test or heart rate monitor availability, for more practical use. Test explanations, preset modules, and preset exercise prescriptions are available online, see link below for more information.

BCTT: https://cdn-links.lww.com/permalink/jsm/a/jsm_2020_01_28_haider_19-313_sdc1.pdf

BCBT: https://cdn-links.lww.com/permalink/jsm/a/jsm_2020_01_28_haider_19-313_sdc2.pdf

Aerobic exercise prescription after BCTT or BCBT:

https://cdn-links.lww.com/permalink/jsm/a/jsm_2020_01_28_haider_19-313_sdc3.pdf

Aerobic exercise if HR monitor is not available:

https://cdn-links.lww.com/permalink/jsm/a/jsm_2020_01_28_haider_19-313_sdc4.pdf;

https://cdn-links.lww.com/permalink/jsm/a/jsm_2020_01_28_haider_19-313_sdc5.pdf

Aerobic exercise prescription if no threshold test is performed:

https://cdn-links.lww.com/permalink/jsm/a/jsm_2020_01_28_haider_19-313_sdc6.pdf

3.5 Vestibular rehabilitation

If vestibular symptoms are present and a vestibular clinical profile is recognized, a vestibular evaluation and rehabilitation are recommended. Studies evidence that an intervention before 30 days from the injury is indicated [48], but it can be started sooner.

The vestibular system is a complex circuit that detects the motion of the head in time and space and helps to regulate postural stability and balance (vestibulo-spinal reflex), and stabilizes vision (vestibulo-ocular reflex). Disruptions to this system due to concussion are frequent [49], in fact from 23% up to 81% of concussed patients experience dizziness [50].

The reason is likely due to a complex and massive interaction of neurons engaging long pathways, including cortex, brainstem and reticular formation, cranial nerves, and peripheral organs.

Symptoms reported are vertigo, dizziness, impairment in balance, in gait and visual motion sensitivity. Visual motion sensitivity refers to an inability to centrally integrate visual and vestibular information, in particular, in busy environments, such as shopping malls. To make the pathology more complex, this dysfunction may be accompanied by anxiety [51]. Alteration in visual and spatial orientation is identified as a cognitive component of vestibular impairment, as the system is also connected to cortical areas.

Usually, these symptoms are recalled under the term “post-concussion dizziness” or “post-traumatic dizziness,” as part of the post-concussion syndrome. It is unclear, to our knowledge, if it is due to functional microstructural abnormalities from the trauma or whether there is an unrecognized labyrinthine cause, or both of them. Autonomic dysfunction could be a potential contributor to post-concussive dizziness, too.

Thus, the necessity of a specific evaluation of the vestibular system, before setting up the rehabilitation program, is mandatory.

If the patient reports spinning vertigo, a labyrinthine cause should be evaluated with specific testing as caloric testing, postural testing, audiometry, and VEMPs, to ensure the correct function of the semicircular canal and otolith organs [49].

If a labyrinthine cause is identified, the treatment aims to resolve the underlying cause. For example, benign paroxysmal positional vertigo (BPPV) should be identified and treated as soon as possible, while possible ruptures of portions of the membranous labyrinth, bleeding, traumatic ischemia, utricular and saccular injuries, and perilymphatic fistula should be addressed to a specialized ENT doctor [49].

If a labyrinthine injury is not identified, the hypothesis of microstructural dysfunction of the brain is reasonable, and symptoms are due to the inability to integrate visual, proprioceptive, and vestibular information. In this latter case, the literature provides some easy and practical tests to assess vestibular and oculomotor function as the Vestibular-Ocular-Motor Screening test [51, 52, 53].

Therapies for vestibular impairment are a group of active treatments, including dynamic movements involving head and eye coordination, balance and gaze stabilization exercises. These therapies are based on an expose-recover model involving exercises that stress specific impairments and make symptoms arise in a controlled way to promote recovery.

Rehabilitation interventions were designed to work on vestibular-ocular reflex impairment improving gaze stability and eye-head coordination, thus promoting habituation and adaptation to dizziness symptoms.

Different vestibular rehabilitation techniques may be used based on the symptoms and impairments. Here, we list the main group of clinical impairments and symptoms and the type of physical interventions [50, 54, 55]. Vestibular-ocular reflex (VOR) impairment contributes to dizziness, vertigo, disequilibrium, visual motion sensitivity, unstable sensations, oscillopsia, impaired fixation, visual tracking, instability, and blurred vision [56]. It can be improved by targeted eye-head coordination and gaze-stability training.

• Eye and head coordination exercises are based on holding the eyes on a fixed target while moving the head up and down or side to side. Progression of the exercise is made by symptoms exacerbation and adding complexity to the exercises as it can be done sitting or standing, walking or jumping.

• Gaze stability training is a group of exercises in which the patient is asked to hold the eyes on a target, as above, but the target could be in motion or different targets are proposed, adding smooth pursuit and saccadic eye movement to the previously described exercises.

• Vestibular-ocular reflex cancelation is based on the ability to inhibit vestibular-ocular reflex. The eyes are fixed on a target while moving the head, but the target is moving in the same direction and speed of the patient’s head.

• Visual motion sensitivity dysfunction is related to symptoms when exposed to environments with complex visual stimuli. It depends on an altered integration of vestibular and visual information and on the alteration of the optokinetic mechanism (see below). A graded and systematic exposure to visually stimulating environments is often used as a rehabilitative technique to habituate the individual and train the system. In the office visual exposure to rotating and confusing backgrounds are used too.

• Balance dysfunction is based on an altered vestibulospinal reflex or proprioceptive deficits, it can be tested in the office with some practical and easy tests, such as Fukuda, Romberg test, Balance Error Scoring System Tests, or Sensory Organization Test.

• Balance training includes sensory proprioceptive training and dynamic balance training. Progression could be made based on the patients’ symptoms by changing position (sitting or standing), changing floor hardness or stability (proprioceptive rocker board or ball), narrowing the base width, standing on one leg, closing the eyes, or confounding glasses may be used to treat impaired postural control. Walking, running, and jumping are used to increase the difficulty and as aerobic stress. Also, head movements could be added.

Many studies have shown that vestibular rehabilitation is effective [57, 58, 59, 60, 61].

If post-traumatic dizziness is persistent despite rehabilitation, other causes should be examined as, for example, cervicogenic dizziness, anxiety-related dizziness, post-traumatic migrainous-related dizziness, or a more serious underlying diffuse axonal injury (DAI). DAI is usually reported in more severe traumatic brain injury, but it has to be taken into account as central nervous dizziness is possible and, if clinically suspected, a diffusion tensor imaging or advanced fiber tract MRI has to be considered [49].

3.6 Visual and ocular-motor rehabilitation

As for every specific rehabilitation protocol, it is important to collect a good clinical anamnesis and physical examination. It will not be discussed as it is not the aim of this chapter, but abnormal findings will guide in the correct rehabilitation approach. Clinicians should remember that particular abnormal findings in vision and ocular movement, such as visual field loss, cranial nerve palsy, and diplopia, should be investigated with brain MRI, unless made before, to exclude the diagnosis of a major brain injury, instead of a concussion [62]. Especially in patients with prolonged symptoms and recovery.

The visual system is particularly vulnerable to brain traumas because of the numerous brain pathways, cortical areas, and cranial nerves involved in vision. In fact, usually monocular (nuclear and infranuclear) eye movement, best known as ductions, is normal, while binocular (supranuclear) eye movement, such as smooth pursuit, saccades, and optokinetic nystagmus, has pathologic findings. The reason is supposed to be due to a longer neurologic pathway of control, as said before. The alteration could be found also in vestibular-ocular reflex and vergence movements.

Given the fact that concussion is not related to anatomical damages, visual problems are identified as visual dysfunction that could lead to symptoms, such as blurry vision, difficulty in reading, and light sensitivity, which are a common complaints (35–65%) in post-concussion patients. Visual information processing could also be altered, and thus should be investigated as cognitive impairment [63, 64].

In 2015, a “see to play” protocol was released to help clinicians in rehabilitation prescription for prescription ocular dysfunction, it is based on evaluation and a sort of “one size fits all” treatment, that you can find in the references at the bottom of the page [65].

Below, we report the main pathological findings in visual/oculomotor function in concussed patients and rehabilitation indications for recovery.

• Convergence insufficiency is the reduced ability to converge and is one of the most common concussion visual dysfunctions. It may produce problems with reading, such as diplopia, skipping words or losing one’s place, and becoming more easily fatigued while reading [66, 67, 68].

  • Convergence insufficiency could be treated with specific exercises. There is a magnitude of exercises in literature, but what seems to be more effective is a combination of office-based exercises and home reinforcement. In particular, office-based exercises should be done by an expert optometrist. The specific indication could be found in the CITT protocol [69] and is based on gross convergence exercises, positive fusional vergence exercises, rump fusional exercises, and jump fusional exercises [69, 70].

• Accommodation insufficiency is the reduced ability of the eye to change focus from a distant to a near target and is reported to be as high as 50% in concussed patients. It contributes to binocular visual function and may produce blurry vision with near tasks, as well as headaches, fatigue, and photophobia. It could be associated with convergence insufficiency and pupillary dysfunction [66, 68, 71].

  • Photophobia is related to pupillary dysfunction in a suspected imbalance between the parasympathetic and sympathetic systems. It should be treated with a reduction to light exposure (hat or glasses with low-density (20% light reduction) achromatic tint, and neutral gray. Physical exercise is also recommended for a better autonomic balance.

  • Accommodation dysfunction could be treated with exercises that enhance accommodation. It could be driven by blurry vision, using various magnitudes of positive/negative lenses in a repetitive manner (flippers) and based on the subject’s task performance, the difficulty could be altered by increasing the dioptric power of the lens. Or it could be driven by vergence and proximity. In this case, the exercises could be done monocular or binocular, and progression is made by bringing closer and closer an object asking to focus on it [71].

• Saccades are rapid refixation of eye movements from one target to another generated from the frontal eye field. Both vertical and horizontal saccades are important in most visual tasks, including reading. They are found to be abnormal after concussion in as many as 25–33% of children and adolescents [66, 72].

  • Saccades are usually treated by a workout on rapid eye movements, usually, binocular exercises triggering horizontal, vertical, and near-far saccades are used. Hart chart, visual scanning exercises, reading, or computerized exercises, for example, Sanet Vision integrator or similar are some of the known interventions [70].

• Smooth pursuit are complex conjugate, steady, symmetric eye movement that permit one to follow a target, They require attention, anticipation, and working memory, and thus their pathway is a complex interaction between brainstem vestibulo-oculomotor pathways and cortical neurocognitive pathways. In children and adolescents with a concussion the prevalence is from 33 to 66% [66, 73].

  • Smooth pursuit could be worked out by different monocular or binocular exercises, such as thumb rotation, rotating pegboard, tracking objects, or using a computerized approach, such as Sanet Vision Integrator or similar, in sports field strobe glasses could be used [70].

• Optokinetic nystagmus is a reflexive eye movement driven by the motion of the visual field on the retina and consists of nystagmus with slow phases in the same direction as the moving stimulus and quick phases in the opposite direction. It is currently believed this reflex is generated through the central processing network integrating visual, vestibular, and proprioceptive information. Symptoms related to optokinetic dysfunction could be related to the best known “visual vertigo” or “visually induced dizziness,” dizziness that appears during exposure to environments with complex visual stimuli (e.g., supermarket aisles) [74].

  • Treatment of these symptoms is frequently connected to vestibular rehabilitation discussed before and it is based on an “expose and recover” approach. In-office treatment is usually made in a room free from points of reference and the visual stimulus should reproduce the appearance of the optokinetic disk (optokinetic rotatory disk, or confounding background movements while gaze is maintained on a fixed dot or figure). Usually, real-life exposure to environments with complex visual stimuli is also performed [75].

• Vestibular-ocular reflex is a reflexive eye movement in relation to head movement as rotations, tilt, or extension. It is fundamental for gaze stabilization and its dysfunction could lead to different symptoms, such as blurred vision, dizziness, vertigo, balance-related symptoms. Due to the multiple structures involved in these reflexes’ pathways, it has a high prevalence in concussed patients.

  • Its rehabilitation has been deeply analyzed in the previous paragraph [56].

Usually, in concussed patients, multimodal exercises are proposed and the result is a mixture of the previously listed exercises, such as saccadic eye movements, visual pursuit, tracking tasks, alternating monocular and binocular tasks, and reading tasks. In addition, visual attention tasks, such as visual-field scanning, attentional grid, and near-far-vision focal shifting, may also be used. Often these tasks involve the use of prisms, special optical lenses, eye cover-ups, penlights, and mirrors. The effectiveness seems to be higher if multiple domain exercises are prescribed [51, 76].

3.7 Cervical rehabilitation

Cervical or neck injury can be defined as persistent impairments caused by dysfunction of the somatosensory system of the cervical spine likely caused by strain on the soft tissue.

Most cervicogenic symptoms have been attributed to injury or impairment of the upper cervical spine. The reason is that afferents from the upper cervical spine (C1-C3) are widely interconnected. They carry somatosensory information of head and neck position to the brainstem and the cerebellum, useful for adaptive postural and oculomotor regulation, and to the thalamus and the primary somatosensory cortex, useful for the perception of head and body position.

In fact, their direct interactions with the vestibular nuclei, superior colliculi, and central cervical nuclei help coordinate important reflexes (cervico-ocular reflex and vestibulo-ocular reflex) required for gaze stabilization during functional head and neck movements, and for postural stability (cervicocollic reflex and vestibulocollic reflexes). In addition, interactions with the spinal tract contribute to postural tone regulation (cervicospinal and vestibulospinal reflexes).

During concussion, especially if caused by a whiplash movement, abnormal somatosensory afferents arising from the muscle spindles, nerve roots, and joint and pain receptors of the cervical spine could determine cervicogenic pain, dizziness, disorientation, blurred vision, and balance problems. Aberrant cervical somatosensory information may directly affect the cervical and vestibular reflexes and ocular responses, or may indirectly affect the system by creating mismatched information between abnormal somatosensory cervical information and normal vestibular and visual information. Moreover, cervical afferents interact with the trigeminal sensory afferents through the lesser and greater occipital nerves and could lead to hemicranial pain [77, 78, 79, 80].

Cervical spine physiotherapy intervention has been demonstrated to be effective in concussion rehabilitation and symptom improvement [81, 82].

Rehabilitation intervention included manual therapy of the cervical and thoracic spines, cervical neuromotor training exercises, and sensorimotor training exercises. It is important that such a program does not produce an increase in pain or headache, but that some temporary exacerbation of dizziness, nausea, unsteadiness, and/or visual disturbances is acceptable [82].

It is important to perform a good physical examination in order to understand if pain originators, muscle hyperactivation, and nerve sensitization are present and to address rehabilitation. If dizziness is present, it is important to understand if it is originated from the cervical spine by performing specific tests, for example, cervical joint-reposition error test, smooth-pursuit neck-torsion test, head-neck differentiation test, cervical flexion-rotation test, and motor-control assessment of deep cervical flexors and extensors [78].

Cervical pain could be discogenic or due to muscle contraction and nerve sensitization. Manual therapy of the cervical and thoracic spines should be addressed based on physical examination and include a set of manipulative therapy for pain, muscle de-contracture, decreasing unwanted muscle activity, and range of movement improvement and relaxation, which are demonstrated to improve patients’ symptoms and joint position sense and dizziness [82, 83].

• Cervical neuromotor training exercises and cervical muscle training have been suggested to improve balance proprioceptive neuromuscular facilitation, for example, activating the deep cervical flexors and scapula stabilizers [82, 84].

• Sensorimotor retraining exercises are a set of specific neuromuscular control exercises to improve cervical joint position sense, head relocation accuracy, and movement sense. It could be trained by using exercises with auditory or visible feedback as a laser fastened to the head to trace patterns on a wall, such as a figure-of-eight. It is important to work also with posture, in particular, by giving ergonomic and postural advice for work sitting position [82].

The best evidence of concussion rehabilitation programs is performing a mixture of vestibular, ocular, and cervical exercises, as they are strictly interconnected [51].

3.8 Post-traumatic headache: non-pharmacological treatment

Post-traumatic headache (PTH) is one of the most common sequelae of traumatic brain injury. It is considered a secondary headache defined by the onset of a headache within 7 days following trauma or injury. If the headache persists beyond 3 months, is it defined as a persistent post-traumatic headache. PTH could be associated with somatic symptoms, for example, nausea, vomiting, photophobia and phonophobia, and cognitive and psychological symptoms.

Possible mechanisms of PTH include trauma-induced impairment in descending modulation of pain-modulating systems, neurometabolic changes, and activation of the trigeminal sensory system. We should also remember that Nociceptive input from upper cervical afferents might also converge on the trigeminocervical complex.

It is important to understand if PTH is a tension-type headache, cervicogenic headache, or a migraine, because treatment interventions could differ. ICHD-3 criteria for diagnosing tension-type or migraine are clear. In the diagnosis of PTH, it is also fundamental to reveal the possibility of co-occurring medication-overuse headaches (MOH), which are frequent and have to be addressed.

The heterogeneity of the headache phenotype in PTH might partially be explained by genetic predisposition and a history of headaches [85, 86].

If a headache or migraine clinical profile is suspected then setting a specific treatment is important in concussion rehabilitation.

The approach to the treatment of post-traumatic headache is both pharmacological and non-pharmacological approaches. In this paragraph, we will list the non-pharmacological intervention, as pharmacological treatment is not the aim of this chapter.

• Lifestyle modifications are important to avoid headache triggers. A headache diary is a helpful tool to aid patients in identifying particular triggers and documenting therapeutic responses. Typical lifestyle modifications are: having regular meals and sleep schedule, avoiding alcohol, chocolate, artificial sweeteners, excessive caffeine intake, managing stress, having good hydration, and performing light aerobic exercise [87].

• Other therapies are relaxation training, thermal biofeedback, and cognitive-behavioral therapy. Cognitive-behavioral therapy (CBT) refers to cognitive processes that help in the resolution of psychopathology, particularly emotional pain and dysfunction. It enables patients to develop preventive and acute care strategies, such as trigger identification, modification of maladaptive interrelated thoughts, feelings, and behaviors, surrounding headache, and physiological autoregulation strategies [88].

• Cervical rehabilitation is beneficial in tension-type headache, but also in cervicogenic headache and migraine that have a hyperactivation of the trigeminal system triggered by afferents from the upper cervical spine [89].

3.9 Cognitive impairment: indication for rehabilitation

Cognitive complaints following a concussion are frequent and include mental fogginess, feeling to be mentally slow down, difficulties with attention and concentration, and memory problems. They may also be exacerbated by emotional symptoms, such as anxiety, irritability or depression, sleep disturbances, and pain.

Cognitive functions are a group of brain superior functions, including memory, visuospatial orientation, attention, learning, information processing capacity, and reaction time. The most frequently affected domains after a concussion are memory, attention, and visuospatial functions [90, 91].

Cognitive impairments are due to the well-known energy crisis of the brain, which is incapable of providing good interaction between complex neural circuits from different brain areas. In literature, there is also evidence in support of a diffuse axonal injury as an anatomical substrate underlying cognitive dysfunction [90], and depending on the extent and distribution of damage multiple sensory, motor, emotional, and cognitive systems can be affected [92].

Even if most of the studies demonstrate that cognitive impairments are acutely associated with concussion, there is also evidence that usually they improve 2 weeks post-injury. Nevertheless, there is less agreement in the literature on when these deficits completely resolve, and there is evidence that some cognitive deficits can last more than 6 months [93]. Moreover, studies conducted on long-term sequelae in concussed patients reveal that cognitive impairment could arise as a summation of multiple concussions [94].

It is mandatory to remember that during the acute phase of concussion, cognitive symptoms may be due to other concomitant causes, such as visual ocular-motor deficits, which could lead to blurred vision and difficulty in reading and focusing; post-traumatic headache that could be triggered by visual stimuli and so pushing the patient to avoid cognitive activity as a way to reduce pain; vestibular and visual vertigo lead the patient to avoid crowded places and has a high relationship with anxiety, which could arise cognitive issues; vestibular impairments are also related directly to visual and spatial orientation; and finally, autonomic dysfunction could provoke fatigue and difficulty in concentrating.

Knowing this interaction between neurological systems is important to address rehabilitation.

In the acute phase and initial cognitive rest is recommended for 48 hours, then an active approach could be initiated.

Cognitive rest includes reducing reading, computer use, texting, watching television or movies, playing video games, and similar mental activities. Complete cognitive rest is impractical and is not advised [95].

Then, a progressive return to the activity of daily living, return to school and work is recommended, it has to be taken as an “expose and recover” mental exercise, so accommodation could be necessary (see below). Treatment should also focus on the ocular, vestibular, cervical, and autonomic system to reduce cognitive cross-linked symptoms.

If cognitive impairments last longer than 2–4 weeks, a specific cognitive rehabilitation should be activated. If psychological health disorders are coexisting, adding cognitive behavioral therapy is suggested.

• Progressive return to learn and work:

Following a concussion, the active return to school and work is recommended to improve cognitive impairments and thus is a major priority for the recovering patient. Moreover, prolonged absence from school or work environments must be avoided to reduce the risk of secondary adverse social and emotional effects, for example, anxiety and depression [9].

Patients returning to school/work while recovering from concussion benefit from individualized management strategies, as concussion symptoms and cognitive impairments have an impact on academic learning and work performance [9]. Accommodative support and adjustments may be necessary to balance the goals of recovery and return to productivity, but it is also important to ensure that modifications are not prolonged when no longer necessary.

Accommodations for cognitive impairment for example are:

• Gradually school and work reentry, extra breaks or flexible work hours.

• Extra time for test assignment/task completion.

• Enhanced level of supervision, help taking notes, or recording classes/meetings.

• Increase repetition in assignments.

• Break assignments down into smaller pieces and deadlines.

• Provide alternate methods for the student to demonstrate mastery, such as multiple-choice.

• Temporary workload restrictions or placement in a completely different job function.

General accommodations, for example, are:

• Modifications in the school environment to reduce triggers for their symptoms, such as removal from gym or dance class, band/orchestra to reduce visual vertigo or headache, or avoiding bright light or loud noises places.

• Decreased computer work and screen exposure.

Literature proposed different return-to-learn and work strategies, for example the “return-to-learn protocol” proposed by Gioia [96], which is similar to the one used for return-to-play mentioned before in this chapter. Some organizations also released guidelines to help clinicians and school professionals with the management of their concussed students or workers [97, 98].

• Cognitive rehabilitation:

It refers to a set of interventions that aim to improve a person’s ability to perform cognitive tasks by retraining previously learned skills and teaching compensatory strategies.

A neuropsychological assessment is fundamental to identify cognitive strengths and weaknesses and areas of treatment. The neuropsychological assessment is usually done by a neuropsychologist with paper and pencil battery tests. In recent years, many computerized neurocognitive testing, designed for concussed patients are at disposal and if specific training is present, they can be evaluated also by clinicians with different specialties [99, 100].

• Cognitive retraining is focused on restoring impaired skills through training specific domains and improving general intellectual and executive functioning, attention, memory, and processing speed. Attention exercises engage both visual and auditory skills. Attention and information-processing exercises are designed to enhance information retention and recall, contributing to improvements in memory and processing speed.

• Cognitive compensatory strategies are the addition of strategies to bypass the cognitive impairment. The key is achieving improved function through the use of an additional tool, for example, using a calendar to remember deadlines, bypassing memory impairments.

• Cognitive-behavioral therapy:

It is a talking therapy that can help patients in managing problems by changing the way they think and behave. It focuses on treating psychological health disorders, including mood, sleep, and anxiety [101].

3.10 Fatigue, anxiety, and sleep disorder: how to manage

Fatigue is defined as “the awareness of a decreased capacity for mental and/or physical activity, because of an imbalance in the availability, utilization, or restoration of resources needed to perform activities” [102].

In the acute phase post-concussion, more than 70% of patients report excessive fatigue, which can persist for years. It is significantly correlated with anxiety and depression and sleep disturbances [103].

Sleep–wake disturbance and fatigue have been linked also to reduced cognitive functioning [104]. Fatigue and autonomic dysfunction are also correlated [105].

• Fatigue management:

  • Lifestyle modifications are recommended, for example, drinking enough fluids to stay well hydrated, healthy eating habits, getting enough sleep, avoiding known stressors, and avoid alcohol.

  • Physical exercise is helpful in reducing fatigue and sleep disturbances [106].

Mood and anxiety disorders are frequent in post-concussed patients. It could be related to previous psychiatric conditions or to other post-concussion impairments, such as vestibular dysfunction, visual motion sensitivity, migraine and isolation from school work, and social recreational activities.

• Anxiety management depends on symptoms gravity:

  • Mild anxiety could be managed with psychological intervention to gain acknowledgment of the problem, cognitive-behavioral therapy, and behavioral intervention similar to exposure therapy for the treatment of phobias. If psychogenic vertigo is present, vestibular rehabilitation may be recommended.

  • Moderate-to-severe anxiety and particularly if panic attacks are frequent, a psychiatric intervention is also suggested.

Sleep disorders reported in post-traumatic brain injury patients include insomnia and hypersomnia syndromes, circadian rhythm disorders, and sleep-related breathing disorders [107, 108]. The pathophysiology may include disruption of neuronal networks involved in the regulation of the circadian rhythm, but it is also related to other post-concussion symptoms, such as pain, headache, or mood disturbances. Studies demonstrate that there is a decrease in melatonin as a possible cause for circadian rhythm alteration. A lack of good-quality sleep is related to fatigue and can affect mood and cognitive functions.

• Sleep management:

  • During the first 48 hours after concussion, sleep is permitted as needed.

After the first few days, avoiding naps and having sleep habits are suggested. For example, having regular bed and wake times and a bedtime routine, such as a warm bath, is helpful. Also, having a healthy sleeping place (dark, clean, tidy, and quiet) is useful. Patients should avoid other activities at bedtime, such as reading, watching TV, or using the computer.

Eating foods containing magnesium, iron, and B vitamins, which could help in producing melatonin, instead of exciting food such as sugar and caffeine 4 to 6 hours before bed, is recommended.

Physical aerobic exercise is suggested everyday, but patient should avoid exercising too close to bedtime.

• Mindfulness therapy and acupuncture could help in some cases.

• Pharmacologic treatment is sometimes recommended if sleep disturbances persist. It could be addressed to treat sleep disorders or the underlying cause as migraine or neck pain.

4. Conclusion

A concussion is a heterogeneous and complex syndrome resulting from acute brain trauma. Most of the symptoms reported are related to a brain energy crisis and to disruption in neural circuits. It is considered a reversible condition, even if some studies demonstrate concussion-related cognitive long-term effects and a suspicion of an underlying diffuse axonal injury is reasonable, as demonstrated in multiple research papers. The summation of a new concussion could lead to phosphorylated tau protein deposits and encephalopathy.

Symptoms usually recover in a brief period, from 2 weeks for adults to 4 weeks for children and adolescents, in almost 80% of cases, but they can last longer. Limiting cognitive and physical rest and setting an early active rehabilitation intervention is the key to a rapid recovery and limiting symptoms chronification.

Progressive cognitive and physical activity in a sub-symptoms threshold manner is the main effective intervention proposed nowadays. In recent years, more individualized rehabilitation is taking place with promising results in concussion management. Clustering patients in different clinical profiles based on individual symptoms lays the foundation for a specific rehabilitation: vestibular, visual ocular-motor, cervical spine, and cognitive rehabilitation are the cornerstone of a tailored intervention. Managing factors, such as mood and anxiety disorder, sleep disturbances, and fatigue, are also fundamental for the achievement of physical and mental well-being.

A concussion is an evolving burning issue and the world of research is moving faster to better understand the importance of concussion clinical profiles, the predictive power of biomarkers, and the effectiveness and timing of treatments.

Conflict of interest

The author has no conflict of interest.