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6. Persistent Post-concussion Symptoms and Long-Term Sequelae
Keywords
Mild traumatic brain injury (mTBI)ConcussionAthletePost-concussion syndromeProlonged recoveryCervicogenic headacheExercise intoleranceVestibular therapySub-symptom threshold exercise trainingChronic traumatic encephalopathyIntroduction
The majority of athletes recover from a concussion within a typical time frame. However, approximately 10–30% of athletes who sustain a concussion will experience a prolonged recovery [1]. There is no universal standard definition for persistent post-concussion symptoms. The Berlin Consensus statement defines persistent symptoms following a concussion as those lasting longer than 2 weeks in adult patients and longer than 4 weeks in pediatric patients, while the Centers for Disease Control and Prevention defines prolonged post-concussion symptoms as lasting longer than 1–3 months after the injury [2, 3]. Prolonged symptoms are not thought to be caused by a single pathological process within the brain, but rather a collection of a variety of symptoms that are often complicated by pre-existing and noninjury factors [3]. As such, athletes with prolonged recovery benefit from a multidisciplinary treatment approach to address their various symptoms [4].
Risk Factors for Prolonged Recovery
No two concussion recoveries are the same, even in the same individual; therefore, predicting precise recover y time is challenging. Nonetheless, there are some factors that have been shown to increase the risk for longer recovery including: history of previous concussion, neurological or psychological disorder, learning difficulties, family and social stressors, and increased concussive symptoms at baseline (pre-concussion) [2, 3]. Post-injury symptoms that have been associated with increased likelihood of prolonged recovery include dizziness, headaches or migraines, initial severity of cognitive deficits, deficits in oculomotor function, and development of depressive symptoms [3]. Risk factors for development of depressive symptoms and other mood disorders in elite and professional athletes include performance expectations, worries over career security, contracts, privacy of condition, and retirement from sport [5]. Some studies also found that women report symptoms for a longer period compared to men, and adolescents are at higher risk for prolonged recovery compared to other age groups [4]. Of all of these factors, pre-existing anxiety and high symptom load immediately after injury have been shown to be the most consistent predictors of prolonged recovery across all studies [3, 4].
How a concussion is initially managed may also influence recovery time. Athletes who stop playing immediately after the injury seem to recover faster than those who continue to play immediately after the injury [6]. Similarly, those who initiate physical and cognitive rest immediately after the injury have shorter recovery times than those who delayed rest for 1–7 days after the injury [7]. It is important to note that prolonged strict rest (more than a few days) after a concussion is associated with longer recovery times and therefore is not recommended [4]. An undiagnosed and therefore untreated concussion can also lead to prolonged symptoms [3]. Suffering another blow to the head while recovering from a concussion can increase the risk for prolonged symptoms. The brain has an increased vulnerability following an initial head injury which can result in more severe and prolonged concussion symptoms and worsened metabolic changes when a second injury is sustained [4]. In addition, athletes who receive a second blow to the head while still recovering from a concussion are at risk for “second impact syndrome .” Although very rare and mostly documented in individuals of high school age and younger, second impact syndrome results in cerebral vascular congestion, diffuse edema, and death [8]. This is why current consensus guidelines emphasize no return to play on the day of injury, and that athletes must be completely recovered and back to their pre-concussion baseline before they can safely return to contact sports and other activities that pose a risk for head injury [3, 4, 8].
Treatment
Even in a patient with a known concussion, it is important to obtain a comprehensive history and physical exam looking for other etiologies of symptoms. Athletes reporting migraines or headaches should be evaluated for pre-existing or underlying disorders and have a thorough evaluation of their cervical spine for cervicogenic cause [4]. Due to the myriad of symptoms experienced by athletes during their recovery, often a variety of treatments are needed to address their persistent symptoms. Treatment is therefore symptom-focused and can include cervical spine rehabilitation, sub-symptom threshold exercise training, vestibular and visual therapy, cognitive behavioral therapy, academic adjustments, lifestyle changes involving sleep, nutrition, and hydration, and rarely, pharmacologic treatments [3].
Cervical Spine Rehabilitation
It is not uncommon for the cervical spine to be injured at the time of a concussion, especially with whiplash type injuries. Missed diagnoses of other injuries inevitably lead to persistent symptoms from misdiagnosis. Dysfunction in the upper cervical spine can cause cervicogenic headaches leading to prolonged concussion headaches [9]. Physical therapy programs targeted at cervical spine dysfunction and have been shown to assist recovery in those with persistent post-concussion symptoms [4]. Cervical spine rehabilitation should include stretching and soft tissue massage to improve cervical muscle flexibility and reduce myofascial trigger points, as well as strengthening exercises and posture training. Modalities such as electrical stimulation and ultrasound may also be helpful.
Sub-symptom Threshold Exercise
An active rehabilitation program that includes limited aerobic exercise is a safe and effective treatment for athletes experiencing persistent symptoms [3, 4]. A unique feature of athletes with persistent concussion symptoms is that they often demonstrate physiologic differences when undergoing aerobic exercise, compared to non-concussed patients. Specifically, athletes with persistent symptoms report higher levels of perceived exertion and have lower heart rates during exercise [1]. Individuals who experience symptoms at a lower heart rate during sub-symptom threshold exercise testing take longer to recover compared to individuals that are able to tolerate exercising at higher heart rates [5]. An athlete has exercise intolerance when they cease exercise due to increase in symptoms at a submaximal intensity and have not yet reached exhaustion or maximum age-predicted heart rate [10]. The most studied test for measuring post-concussion exercise tolerance is the Buffalo Concussion Treadmill Test (BCTT). After establishing an athlete’s aerobic tolerance using the BCTT, a structured aerobic exercise program, such as the Buffalo Concussion Exercise Treatment protocol, can be used to progressively increase their aerobic tolerance [1, 4]. For athletes who may not have access to skilled provider who can administer the BCTT and exercise protocol, healthcare providers can advise athletes to engage in light aerobic exercise for 20 min and to cease exercise sooner if their symptoms increase more than two points from baseline (on a ten-point scale) [10]. In addition to facilitating recovery, sub-symptom threshold exercise training programs can also minimize physical deconditioning, while the athlete is resting from his/her sport [1].
Vestibular and Visual Therapy
Vestibulo-ocular dysfunction has been shown to be prevalent in patients with prolonged concussion symptoms [1]. Vestibular-Ocular Motor Screening (VOMS) is a clinical tool to evaluate oculomotor function and symptom provocation with ocular movements. VOMS assessment includes smooth pursuits , horizontal and vertical saccades, vestibular ocular reflex, near point of convergence, and visual motion sensitivity [4]. Mucha et al. provide a detailed description of how to administer VOMS in the setting of concussion [11]. Patients with persistent symptoms usually have difficulty with one or more of these ocular movements or experience symptom provocation during VOMS testing [4]. Individualized visual therapy is often helpful for these patients and can include exercises to retrain visual skills such as convergence, focus, tracking, and eye teaming.
Vestibular deficits may also be seen in patients with persistent symptoms. These may include difficulty with tandem walking, positive Romberg test, motion sickness, or symptoms of dizziness or nausea with positional changes. Vestibular therapies expose impairments with symptom provoking maneuvers in a controlled manner and direct the athlete’s rehabilitation with focus on dynamic movements that cause an increase in symptoms [12]. Physical therapy programs targeted at vestibular dysfunction have been shown to facilitate recovery, specifically improving balance and reducing dizziness, in those with persistent post-concussion symptoms.
Academic Adjustments
Concussions can have effects on cognition including attention, memory, and executive function difficulties. Particularly in collegiate and high school athletes, memory difficulties, slower processing speed, and executive dysfunction interfere with learning and can negatively impact academic performance. These difficulties are often distressing for the student and can lead to significant anxiety which can compound the symptoms further. An individualized return-to-learn plan can help athletes with persistent symptoms continue to learn and succeed academically during their recovery [4]. It is important for the treating physician to get specific details from the athlete about which cognitive tasks they are struggling with so that an individualized academic plan can be developed and shared with the school and teachers. Athletes may have difficulty advocating for themselves when communicating with teachers, so providing this support for them and communicating with school administrators and teachers can be essential in reducing their anxiety about falling behind academically.
Sleep Hygiene and Nutrition/Hydration
Athletes with persistent symptoms often experience one or more symptoms related to sleep such as difficulty falling asleep, daytime sleepiness, or sleeping more or less than usual. This can be problematic as getting adequate sleep is important to concussion recovery. As such, athletes should be counseled in sleep hygiene, including maintaining consistent sleep and wake times each day, limiting naps to 20–30 min to avoid interrupting nighttime sleep, and turning off electronics at least an hour before bedtime. Proper nutrition and hydration are frequently overlooked by athletes during concussion recovery, especially when they are not training intensively for their sport every day as they typically do when they are uninjured. Headaches and dizziness can be exacerbated by dehydration and low blood sugar, so they must pay careful attention to adequate hydration and eat small frequent meals that include protein, complex carbohydrates, and fruits and vegetables and are low in added sugar and unnecessary additives/preservatives.
Psychological Counseling and Cognitive Behavioral Therapy
Patients with prolonged symptoms are often frustrated that they have not yet recovered and may develop symptoms of anxiety and depression. Referral to a clinical psychologist can be very helpful as they can provide stress management strategies, relaxation techniques, and supportive counseling . They can also screen for more severe mood symptoms and refer to a psychiatrist for pharmacologic management if warranted. Cognitive behavioral therapy (CBT) , a form of psychotherapy which aims to modify dysfunctional thinking and beliefs, has recently been shown to help patients with prolonged recovery manage their symptoms [4].
Pharmacologic Treatments
There is insufficient evidence to support the use of pharmacologic treatment of concussion symptoms [3]. A systematic review found no convincing evidence to support use of peripheral nerve blocks, amitriptyline, and amantadine in the treatment of persistent symptoms [1]. It is important to note that if an athlete is prescribed a medication for a persistent concussion symptom, they should be weaned off the medication and be symptom-free prior to returning to their sport [3]. Medication-overuse headaches can be caused by long-term use of nonsteroidal anti-inflammatory medications and acetaminophen, and therefore chronic use of over the counter analgesics should be discouraged [8].
There has been no research on humans to show that any nutritional supplements can prevent or treat concussion symptoms [4, 8]. Additionally, they are not FDA regulated and therefore have potential for harm or contamination. As a result, using supplements in the treatment of concussion is not recommended [4].
Prevention of Persistent Symptoms
Participation in both physical and cognitive activities should be limited in the first few days following a concussion. Then the athlete’s usual activities should gradually be resumed as tolerated as long as they do not increase the number or severity of symptoms. This includes engaging in light aerobic activity as tolerated. In fact, early individualized sub-symptom threshold exercise training may reduce chances of prolonged recovery from concussion in athletes [13]. Prolonged strict rest can increase symptom burden [2].
Retirement from Sport
There are no evidence-based recommendations to guide physicians and athletes regarding retirement or extended breaks from contact sports in the setting of concussion. Current recommendations are based on expert opinion. Consideration for retirement or an extended break from contact sports should not be based solely on the number of concussions, but rather on the quality of recovery from each concussion. As such, factors that should prompt a discussion and consideration of extended time off from contact sports include persistent post-concussive symptoms, worsening symptoms with each subsequent concussion, repeated concussions occurring with lesser and lesser force, persistent deficits on neurologic exam or neuropsychiatric testing, certain traumatic structural injuries or abnormalities on neuroimaging (e.g., large arachnoid cyst, intracranial hemorrhage, or Chiari malformation), and decline in academic or athletic performance. An athlete’s readiness to return to sport should also be considered after each injury [4, 5]. Any decision regarding retirement or extended break rest from contact sports should be evaluated on an individual basis and include a comprehensive discussion with the athlete and multidisciplinary medical team of the long- and short-term benefits and risks of continued participation in contact sports.
Long-Term Sequelae
Recently, there has been significant concern about the potential long-term effects of repeated concussions on cognitive function and emotional health [8]. Small autopsy studies of mostly former professional contact-sport athletes who had sustained numerous concussions have demonstrated deposition of hyperphosphorylated tau (p-tau) protein around small blood vessels of the cortex, typically at the sulcal depths. This has been labeled, “chronic traumatic encephalopathy” (CTE) . CTE can only be diagnosed on a postmortem autopsy. Currently, there is no way to conclusively diagnose CTE in a living individual [8]. Additionally, a cause and effect relationship between CTE found on autopsy and behavioral changes, mood disorders, or cognitive difficulties during life has not been demonstrated [3, 4]. Further research is needed to determine what factors may predict or predispose an individual to permanent or long-term sequelae after a concussion [3, 4, 8].
Expert Opinion
Approximately 10–30% of athletes with concussion will experience symptoms that last beyond the expected recovery time period (2 weeks for adults and 4 weeks for children).
The strongest risk factors for prolonged recovery are pre-existing anxiety and high symptom load immediately after the injury.
Risk for prolonged recovery may be reduced by removing the athlete from play immediately after the injury, initiating relative physical and cognitive rest for the first few days and then gradually resuming usual activities as tolerated. Resumption of activities should include sub-symptom threshold aerobic exercise which can help facilitate recovery.
Prolonged, strict rest after a concussion is no longer recommended as it has been shown to increase the risk for persistent symptoms. Treatment for athletes with persistent symptoms is symptom-targeted and requires a multidisciplinary approach.
Athletes with persistent symptoms can benefit from cervical spine rehabilitation, sub-symptom threshold exercise training, vestibular and visual therapy, cognitive behavioral therapy, and counseling with regard to sleep hygiene, nutrition, and hydration.
More research is needed to understand the potential long-term effects of one or more concussions on cognitive function and emotional health, who is at risk, and how this risk might be mitigated.
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