Keywordsconcussion, postconcussion syndrome, diagnosis, treatment, chronic traumatic encephalopathy, sports participation, headache
Postconcussion syndrome (PCS) is a common condition that includes physical, cognitive, and affective symptoms. PCS has a long history of controversy, is diagnostically complex, and lacks a widely accepted approach to management. Writings on the subject appear in the medical literature as far back as the late nineteenth century, when Jean-Martin Charcot described twenty cases of “traumatic hysteria.” John Hughlings Jackson and Joseph Babinski followed with seminal works that further elucidated how the interactions between psychologic factors and organic pathologies work to produce self-propagating symptom complexes. These works helped frame the early thinking of this condition, which became known as “shell shock” in relation to World War I soldiers who developed a predictable pattern of chronic symptoms after being in the proximity of an explosion while suffering no observable head wound. The evolution in terminology continued in the mid-twentieth century when the term postconcussion syndrome was popularized, indicating a more complex pathophysiologic process that included, but was not limited to, psychologic mediators. Although the accepted terminology for the condition has evolved over nearly a century, a clear understanding of the etiologies of PCS remains elusive and no single definition of PCS is accepted by the medical community.
Scientific and clinical interest has focused on the consequences of head injuries, particularly those suffered in organized athletics and during the course of military service. In patients suffering a mild traumatic brain injury (concussion), PCS is estimated to occur in 24 to 84 percent of cases. Given that the US Centers for Disease Control and Prevention estimates that between 1.6 and 3.8 million concussions occur in the United States annually from sports and recreation activities alone, the prevalence of PCS is probably high. Traditionally, the diagnosis of PCS has used symptom-based criteria, but the application of a more comprehensive clinical approach is now favored.
PCS has been codified under both the International Statistical Classification of Diseases and Related Health Problems (ICD-10) and the Diagnostic and Statistical Manual of Mental Disorders (DSM-IV). The ICD-10 criteria begin with a history of head trauma “usually sufficiently severe to result in loss of consciousness.” Diagnosis then requires the presence of three or more of the following symptoms: headache, dizziness, fatigue, irritability, insomnia, concentration or memory difficulty, and intolerance of stress, emotion, or alcohol. The sole exclusionary criterion is the absence of an ongoing concussion. This diagnostic schema has come under criticism for three main reasons. First, observational studies have indicated that less than 10 percent of concussions involve loss of consciousness, and its presence is not a predictor of symptom duration. Second, the presence of five, rather than three, of the ICD-10 symptoms has been shown to be diagnostically useful for PCS at 1 month after injury, with a sensitivity of 73 percent and specificity of 61 percent. At 3 months after injury, the ICD-10 symptoms were not found to be useful for making a diagnosis of PCS. The third criticism involves the absence of symptoms that pertain specifically to mood or affect, which are common in PCS.
By comparison, the DSM-IV criteria do include mood- and affect-related symptoms. The DSM-IV diagnostic schema begins with a history of traumatic brain injury causing “significant cerebral concussion.” Cognitive deficits in attention or memory are then required, as is the presence of at least three of the following symptoms: fatigue, sleep difficulty, headache, dizziness, irritability, affective disturbance, personality change, or apathy. Symptoms must also persist for 3 months and interfere with social functioning. Dementing illnesses or other conditions that could account for symptoms need to be excluded. As with the ICD-10 criteria, the DSM-IV criteria are notable for their lack of specific symptoms commonly seen in these patients, namely those of multi-domain cognitive dysfunction. Whether the clinician opts to use the ICD-10 or DSM-IV diagnostic criteria, significant limitations exist. In one study, a consecutive series of 340 patients was evaluated with both criteria; the two criteria resulted in markedly different incidence rates without any discernible pattern to support the clinical utility of either.
Several factors account for the difficulties in applying any strict diagnostic criteria to PCS. The nature of the antecedent event is usually concussion, which itself is a separate clinical entity that has diagnostic confusion and an incompletely elucidated pathophysiology. Given that PCS is a diagnosis preceded by concussion, a certain amount of uncertainty is inherent. PCS-like symptoms may also be present in individuals who have not experienced head trauma. In one healthy, noninjured population, the incidence of reporting three or more typical PCS symptoms was 80 percent. Many common conditions, such as depression, attention-deficit hyperactivity disorder, migraine, and sleep disorders can easily be exacerbated by a preceding brain injury and produce symptoms similar to PCS, creating a complex differential diagnosis.
Given the uncertainty produced through the application of specific, symptom-based, diagnostic schemata for PCS, an alternative approach should be taken that allows for a more open-ended interpretation of PCS symptoms and the use of basic clinical principles to dictate diagnostic accuracy. The clinician must first accurately recognize concussion and identify its resolution, before determining the presence of PCS. Symptoms of prolonged concussion must be distinguished from PCS.
The American Academy of Neurology recognizes concussion as a “clinical syndrome of biomechanically induced alteration of brain function, typically affecting memory and orientation, which may involve loss of consciousness.” In most cases, concussion is characterized by a rapid onset of symptoms or cognitive dysfunction that resolves spontaneously. Concussions typically produce no abnormalities on standard structural neuroimaging, although newer imaging technologies, such as functional magnetic resonance imaging (fMRI), do show promise as potential diagnostic tools. The pathophysiology of concussion is not completely understood but it is assumed to have a significant metabolic component characterized by a mismatch between the amount of energy available to cortical neurons and the amount needed to perform expected neuronal functions and restore appropriate intracellular ion concentrations to their preinjury states. The majority of concussions, perhaps as many as 90 percent, have complete symptom resolution in 7 days. Common manifestations of concussion include physical symptoms such as headache, nausea, and photophobia; cognitive symptoms; emotional symptoms; and sleep disturbance. Loss of consciousness is not required to make the diagnosis and occurs in the significant minority (less than 10 percent) of cases.
The hallmark of concussion management in the acute phase is rest, both physical and cognitive, although there is a lack of published data that point to a particular duration or degree of rest that is beneficial. There is no objective confirmatory test for concussion that is widely accepted, and the recommended clinical approach for determining the resolution of a concussion is for the patient who has recently become asymptomatic to undergo a series of increasing physical challenges, allowing enough time between each challenge (24 hours on average) for symptoms to develop. If the recently concussed patient is able to tolerate significant levels of physical exertion, with heart rate elevated above 80 percent of estimated maximum heart rate for at least 30 minutes, along with complex physical tasks without the return of symptoms, it is reasonable to conclude that the concussion has resolved. The approach of using stepwise physical exertion to determine a return to participation in activities is discussed below.
A minority of concussions will last longer than 7 days. These cases can be attributed to individual variation in some combination of the degree of metabolic injury, the propensity for a particular patient to experience the symptoms of concussion, and the presence of confounding comorbidities such as migraine headache, attention deficit hyperactivity disorder, or depression. It is assumed that continued physical exertion, and perhaps even cognitive exertion, during the acute postinjury phase (2 to 3 days) following the initial head trauma may result in deepening the causative metabolic injury and prolonging the clinical syndrome of concussion. A concussed patient who experiences a second blow to the head or body resulting in an acceleration-deceleration injury of the brain may exacerbate the underlying pathophysiology. In either scenario, the ensuing injury may last significantly longer than the 7-day average, producing a concussion that can persist for several weeks.
PCS is the clinical manifestation of a pathologic process that is separate from concussion and produces a clinically distinct symptom complex. Although the nomenclature of PCS implies that it occurs following the original injury, the pathologic process actually may begin before the associated concussion has completely resolved. While the patient is still symptomatic from the initial injury, it is difficult to determine which process is contributing. PCS symptoms always eventually outlast the symptoms of concussion and become the primary clinical concern.
The precise mechanism of PCS is not well understood but is thought to include both psychologic and organic factors. Postulated organic causes include subcellular structural changes, impaired regulation of cerebral blood flow, and changes in brain network connectivity. Although organic factors have been implicated more closely in the creation of PCS symptoms, psychologic factors may be responsible for their chronicity. The symptoms of PCS are widely accepted to have the potential to last for months or even years.
Regardless of the duration of the preceding concussion, the key to diagnosing PCS is first to determine that the concussion itself has resolved. This can be difficult given that the symptoms of concussion and PCS overlap in character and in timing. A thorough neurologic history that explicitly describes the time course of each symptom is essential. The natural history of concussion symptoms tends to be monophasic, with a gradual and progressive resolution of symptoms over time, allowing for occasional symptomatic worsening with continued exertion or subsequent injury. The timing of PCS symptoms, by contrast, tends to be more variable. PCS symptoms do not respond to continued physical or cognitive rest, whereas rest typically improves concussive symptoms.
In patients with concussion whose symptoms are still present and whose history does not allow for an easy delineation between concussion and PCS, the patient can be asked to increase gradually their physical or cognitive activities while monitoring for changes in symptom duration and severity. PCS responds favorably to a gradual introduction of physical exertion, whereas no such relationship has been described for concussion. Care should be taken not to allow a symptomatic patient who may still be concussed to continue to increase their physical exertion to the point of dramatically increasing symptom severity.
Currently, there are no diagnostic tests that are helpful in making a diagnosis of PCS. Several technologies continue to be investigated including quantitative electroencephalography (EEG), fMRI, and magnetic resonance spectroscopy. Neuropsychologic tests can provide important information including identifying the presence of other comorbid diagnoses but must be used as one part of a larger clinical evaluation paradigm.
Given that PCS has many symptoms and features in common with other conditions, it is frequently misdiagnosed. Some of the more common conditions that should be considered include migraine and other headache disorders, depression, attention deficit hyperactivity disorder, and sleep disorders. Each of these preexisting conditions can potentially be exacerbated by a traumatic brain injury; in some instances, these conditions may only be mild, or even asymptomatic, prior to a concussion and then worsen considerably afterward, leading to diagnostic confusion with the symptoms of PCS.
An alternative approach to this differential diagnosis is to use a more liberal application of the PCS diagnosis itself, allowing for these “comorbid” conditions to be considered subtypes of PCS. In this way, the diagnosis of PCS becomes more simple. The clinician need only determine that the presenting symptoms were not present, or were present to a lesser degree, prior to the inciting concussion and that the concussion itself has resolved. Using this approach, any neurologic symptom-complex that begins following a head trauma and continues beyond the course of the actual concussion may be considered to be part of PCS regardless of symptom number, type, or duration.
One additional symptom-generating mechanism that must be considered carefully is that of inappropriate rest. Having an individual dramatically reduce their level of physical, cognitive, and social activity is a risk factor for the development of physical, cognitive, emotional, or sleep-related symptoms. Identifying rest as a potential contributor to symptoms is important, given that it is also the hallmark treatment for concussion. Symptoms present due to inappropriate rest that are misinterpreted as being direct manifestations of the original brain injury will be made worse if the patient is asked to continue their period of rest. A careful history should include asking about current levels of activity and how they relate to the patient’s preinjury experience.
Treatment and prognosis
Once PCS has been diagnosed, the first step in developing a treatment plan involves addressing suspected symptom generators. If over-resting is suspected, the patient should be instructed to begin gradually reintroducing physical exertion, cognitive exertion, and social involvement. Ignoring this particular potential symptom generator will further propagate symptoms and potentially decrease the efficacy of other treatment modalities.
Preexisting conditions should be addressed and treated symptomatically including migraine and depression. The management of PCS should then turn to addressing the specific symptoms that remain; since there are no pharmacologic therapies specifically for PCS, treatment is analogous to that of common conditions that produce the symptoms in question. Psychologic therapy and cognitive behavioral therapy have some benefit. Hyperbaric oxygen has been suggested as a possible treatment for PCS but its use, as yet, is not widely accepted.
Despite the diagnostic complexities of PCS and a lack of specific proven therapies, prognosis is largely positive, with the majority of patients experiencing complete symptom resolution within 6 months.
Return to participation
One of the most critical decisions in the management of patients with PCS is deciding when to recommend a return to sports, school, or work. This decision is complex, given the multitude of variables that can effect PCS symptom development, severity, and duration. The degree of individual variability in brain physiology, and thus response to injury, can produce different estimations of inherent risk on a case-by-case basis. Differing levels of injury risk that are associated with specific activities in question help to further define future risk of injury; players of American football are likely to be at higher risk of recurrent injury than baseball players. The amount of physical, psychologic, social, or economic benefit that may come from returning to that activity cannot be ignored as these factors define the patient’s personal motivation for returning to participation.
It is essential that the clinician be confident that the patient is no longer concussed as there is clear medical consensus that individuals who are still concussed should not be exposed to additional significant risk of further head injury. Patients who are symptomatic from a concussion should avoid the extremes of physical and cognitive exertion in an effort to minimize symptom duration and severity. The decision to return to participation for a patient diagnosed with concussion involves a relatively straightforward management construct in which the resolution of the injury is determined through a series of increasing physical challenges while assessing for symptomatic worsening. Unfortunately, no similarly accepted approach for returning to play with PCS exists, further highlighting the need to be certain about the diagnosis.
Participation after Concussion
The majority of concussions are self-limited clinical syndromes that resolve spontaneously. It has been estimated that up to 90 percent of concussions in adults will resolve between 7 and 10 days. The risk from returning to a contact-risk activity while still actively concussed is twofold. First, the actively concussed state appears to be a period of increased vulnerability to additional injury, and perhaps to more significant injury. It has been suggested that during this time of physiologic vulnerability, it takes less biomechanical force to produce an additional physiologic perturbation. The diagnosis of “second-impact syndrome” has been used to refer to a potentially devastating, perhaps lethal, state of malignant cerebral edema that is induced when a patient who is actively concussed experiences another biomechanical force acting on their brain. The nature of second-impact syndrome is still unclear, with some authors downplaying the importance of the second impact itself, instead postulating that the condition is a manifestation of an inherent sensitivity, perhaps at the ion-channel level, to any significant biomechanical force. The second reason to limit contact-risk exposure while an individual is still concussed is that additional blows to the head or body that transmit biomechanical force to the brain may exacerbate the existing injury and induce greater symptom duration and severity, resulting in an overall increase in morbidity.
The process for making a return-to-participation decision following concussion begins with the determination that the patient is no longer experiencing the acute symptoms of the injury. Clinicians should be careful not to insist that patients are completely asymptomatic, as the presence of some symptoms may be accounted for by other noninjury factors related to management, such as the loss of physical activity and social interaction. It is more appropriate that the patient be able to tolerate a day of “regular” activities, such as going to school, without a return of bothersome symptoms and without the use of symptomatic medications or other therapies. Once this is the case, it is then best to have the patient begin a graduated set of physical challenges designed to test whether an injury might still exist that is subsymptomatic.
Each stage of the return to participation protocol is designed to test a very particular demand on brain function ( Table 38-1 ). Stage I is designed to introduce simple cardiovascular exertion that is sustained and constant. Around 30 minutes of exertion with a heart rate sustained between 70 and 80 percent of the expected maximum (which can be calculated as 220 minus the patient’s age) is usually adequate. This first stage is best accomplished by the use of a stationary bike, as this minimizes other variables including movement, visual processing, and cognitive load. Stage II adds predictable, simple movement by having the patient jog on a treadmill with the same time and cardiovascular goals as stage I. Stage III adds both complex movements and interval cardiovascular exertion through the use of sport-specific agility drills; this stage can also include resistance training. As with the first two stages, at least 30 minutes of exposure is necessary. Stage IV adds the cognitive load of playing the sport in question, by having the patient participate in a typical noncontact practice that has been carefully controlled to eliminate any significant risk of head trauma. Stage IV further challenges the patient by providing a complex and dynamic visual environment. The final stage is a return to participation without restrictions.