Concussion is the most common head injury in sports. It can be defined as a complex pathophysiological process affecting the brain induced by traumatic biomechanical forces (Figure), and because of unique force vectors, it is differentiated from non-sports related mild traumatic brain injury (mTBI) (31). Most athletes experience a full spontaneous recovery from concussion. However, a clinically significant minority of patients experience postconcussion syndrome (PCS), a complex constellation of symptoms that persists for an extended period of time after the initial concussion. This 5%-20% of concussed patients has been described by some as the "miserable minority" (20,50,28), but given the high prevalence of concussion, a considerable number of athletes each year in the United States may experience PCS (26). PCS has been debated and discussed in the neuropsychiatric literature for some time, but there is scant literature about this diagnosis in the field of sports medicine. Our understanding of athletic concussion is evolving as sports-related studies take place, but present information about PCS is sometimes inferred from non-sports mTBI research. In this article, the controversies and latest science regarding PCS will be reviewed, particularly as it relates to athletes, and a working framework for diagnosis, treatment, and return to play will be explored.
PCS is an ill-defined term. Some physicians may refer to any symptoms experienced by a patient after concussion as PCS; however, there is a normal course of symptom persistence after injury, which generally is followed by gradual resolution. The distinguishing factor between postconcussive symptoms (which are typical after a concussion) and postconcussive syndrome is the length of symptom persistence. Where the normal course of symptom resolution in a concussion should end and where PCS begins is variably defined. The ambiguity in this definition leads to imprecision and variability in interpretation of the literature.
Among the existing definitions, the World Health Organization defined PCS in 1992 as a syndrome that occurs following head trauma (usually sufficiently severe to result in loss of consciousness) and includes three or more of the following eight symptoms: 1) headache, 2) dizziness, 3) fatigue, 4) irritability, 5) difficulty in concentrating and performing mental tasks, 6) impairment of memory, 7) insomnia, and 8) reduced tolerance to stress, emotional excitement, or alcohol (51). The 2007 online update to the ICD-10 removed the need for three symptoms and instead referred to "any number of these disparate symptoms" (51). There is no specification in this definition as to how long symptoms must be present to establish a diagnosis of PCS.
In contrast, the Diagnostic and Statistical Manual of Mental Disorders (DSM-IV) criteria for postconcussional disorder in 1994 (4) incorporates a history of head injury that includes two of the following: loss of consciousness for 5 min or more, posttraumatic amnesia of 12 h or more, or onset of seizures within 6 months of injury. Additionally, there must be difficulty concentrating and learning or memory and three of the following symptoms that appear after injury and persist for 3 or more months: easy fatigability, sleep disturbance, headache, vertigo/dizziness, irritability, anxiety or depression, personality change, or apathy (4).
Neither of these definitions fit well the constructs of PCS in an athletic setting. The DSM-IV head injury criteria are too strict, as 90% of concussions do not involve loss of consciousness (5), seizure disorder is a rare consequence from athletic concussion, and amnesia of even a few seconds has been found to be highly predictive of postinjury neurocognitive deficits (9). The ICD-10 diagnosis is nonspecific because these criteria have not been able to distinguish PCS from individuals with chronic pain, non-brain-injured trauma, psychiatric disease, or minor medical problems (46,19,50,21,10). A reliable and consistent definition is needed to further scientific research and provide clarity to our discussions regarding PCS.
We propose a definition of PCS in athletes as the persistence of cognitive, physical, or emotional symptoms of concussion for a time frame longer than normally would be expected. In athletes with PCS, a diagnosis of PCS can be considered far sooner than the 3-month time frame suggested for mTBI-related PCS. Symptoms persisting anywhere from 1 to 6 wk have been suggested as thresholds for making the diagnosis of sports-related PCS (D. McKeag and K. Harmon, personal communication, October 2009).
PATHOPHYSIOLOGY AND CONTROVERSY
The confusion about a clear definition for PCS and lack of findings on standard imaging has led to a significant debate in the neuropsychiatry literature, with some authors concluding that the persistence of postconcussion symptoms is not a consequence of brain injury but rather is caused by psychological illness (27,33,50). Some literature suggests that even in the absence of preinjury psychiatric disease, the stress of injury results in depression and anxiety, which disrupts concentration and other mental operations (1). In his review, Rees concluded that PCS after mild brain trauma is biologically inseparable from posttraumatic stress disorder (43), and in an opinion article, Wood stated that persistent cognitive symptoms after mTBI potentially are a consequence of pain, not a result of cerebral injury (50). These authors argue that PCS is caused by perceived expectations following head injury, is influenced by poor coping mechanisms, and is prolonged by motivational and financial factors (50). Another author suggested that the use of the term PCS by practitioners leads to attribution error (patients believing that symptoms are caused by mechanical brain injury) and falsely creates an epidemic among patients (33).
On the other hand, Bigler proposed that the biomechanical forces on the brainstem, forebrain, and temporal lobe that occur during brain injury are responsible for the symptoms observed in PCS (3). As discussed later, ongoing research using new diagnostic modalities is finding objective measures of compromised brain function in patients with PCS.
Yeates summed up these conflicting views as "psychogenesis versus physiogenesis" and attributed the controversy to the inconsistent definitions of PCS and the lack of methodologically sound studies. His prospective, longitudinal trial on children found that severity of head injury predicted postconcussion symptoms in most but not all patients, concluding that persistent postconcussion symptoms can result for different reasons in different patients, and thus, each case of PCS should be evaluated independently (52).
In the end, PCS remains a clinical diagnosis arrived at after careful review of a patient's history, and preinjury psychiatric and medical status may influence the outcome of PCS.
PREDICTORS AND RISK FACTORS
Given the high volume of athletic patients with concussion, it would be helpful to understand which factors may predict the subset of patients who are likely to have persistent symptoms. The severity of the initial injury does not necessarily correlate with the significance of symptoms after concussion. A number of recent studies have attempted to look at which factors can predict PCS.
Previous concussion grading systems, since abandoned by the Third International Conference on Concussion in Sport, used loss of consciousness (LOC) as a marker for injury severity, but LOC has been shown to be poorly predictive of symptoms and cognitive disturbance after concussion (45). In 2003, a study by Collins et al. illustrated that amnesia, rather than loss of consciousness, was predictive of postconcussion symptoms in athletes at 5 d after the concussion but did not report on its relationship to symptoms lasting longer (9). Another study found that migraine symptoms and self-reported cognitive decline were associated with prolonged symptoms after concussion (23).
A study of patients with mTBI showed that patients with noise sensitivity in the week postinjury were three times more likely to have persistent postconcussion symptoms at 3 months. Light sensitivity also was a statistically significant risk factor for PCS, but headache, fatigue, and dizziness in the first 10 d after injury did not correlate with patients having PCS at 3 months (12).
Research has been conflicting regarding the role of previous concussions in the development of PCS. Some studies show no relationship between the number of self-reported concussions and current cognitive state (7,47). In contrast, a study by Collins showed that U.S. college football players who had had two or more concussions performed worse on neuropsychiatric measures of executive functioning and speed of information processing (8), and there were similar findings in a study of high school athletes (35). The relationship to the number of concussions and the development of PCS is unknown.
A review by Dick found that female athletes may be at greater risk of concussion than their male counterparts, and McCauley found that women also are at greater risk of developing PCS (11,29). The role of age is unclear, with McCauley finding that this is not a significant risk factor, but a more recent study stating that women have a higher risk of developing PCS than girls (38). An additional finding in McCauley's study was that fewer Hispanic patients met the criteria for PCS than those of other races (29).
Athletes have similar mental health issues as nonathletes, and there are data that confirm the higher incidence of PCS in patients with premorbid psychiatric illnesses, including anxiety and depression and compulsive, histrionic, and narcissistic personality disorders (13). A prospective cohort study of 180 patients found that female trauma patients with anxiety as an initial symptom after mTBI were the most likely to have PCS at 3 months postinjury (12). Studies also have shown that a negative initial perception of injury increases the likelihood of persisting postconcussion symptoms (48).
Litigation also has been proposed as a risk factor for PCS, although data have been mixed (43,13). Except at the professional level, litigation typically is not involved after athletic concussion, and because the primary concern for most athletes is an expeditious return to play, it is unlikely that litigation is a major factor in most athletic concussions.
It is difficult to predict which athletes may develop PCS. Those athletes who experience noise sensitivity, previous migraine headaches, or amnesia may be more likely to have prolonged symptomatology. In addition, athletes with a history of previous concussion and those who have preexisting psychiatric issues could be at higher risk of developing PCS.
CLINICAL FEATURE OF PCS
The list of symptoms experienced with PCS includes persistence of acute concussion symptoms as well as other physical, cognitive, and emotional symptoms (Table).
Physical symptoms of PCS include headache, fatigue and low energy, sleep disturbance, nausea, vision changes, tinnitus, dizziness, light, and photo/phonophobia (22).
Headache is the most common complaint in PCS. The majority of the headaches likely are to be of the tension-type, but a number of other headache types have been implicated in PCS. The parallel pathophysiology of posttraumatic and migraine headache may account for the high prevalence of migraine in patients after concussion (37). A study found that cluster headaches also are present at a higher incidence after head trauma, and occipital neuralgia has been described in PCS (15). Athletes with PCS should be evaluated for other sources of headache, including referred pain from the temporomadibular joint and sinuses, medication overuse, and other forms of chronic headache, which may be amenable to treatment (18). Posttraumatic headache is associated with balance deficits in athletes, and an evaluation of balance should accompany the review of PCS headache (42).
Cognitive symptoms include slowed thinking or response speed, mental fogginess, poor concentration, distractibility, trouble with learning and memory, disorganization, and problem solving difficulties (22).
A player can be free of perceived symptoms but still show cognitive deficits on testing. One small study found that patients with a history of mTBI and PCS had statistically significant worsening of cognitive function in comparison to controls at 4 and 7 months after injury (32). Asymptomatic individuals who do not have cognitive complaints of other PCS symptoms but have decreased measure on neuropsychiatric testing generally are not considered to have PCS.
These symptoms include lowered frustration tolerance, irritability, increased emotionality, depression, anxiety, clinginess, and personality changes (22).
A retrospective review of retired professional gridiron football players found that a history of one concussion did not raise the likelihood of depression in life, but players with a history of three or more concussions were three times more likely to be diagnosed with depression. Of retired National Football League (NFL) players who were diagnosed with postconcussion related depression, 87% continued to have lifelong symptoms (17).
Computed tomography (CT) scan or magnetic resonance imaging (MRI) often are normal in the initial and follow-up evaluations for patients with concussion. Although they are important tests to rule out alternative explanations for the patient's symptoms, they do not have a role in diagnosis of PCS. Recent studies have looked at a number of diagnostic options for PCS including functional MRI (fMRI), magnetoencephalography (MEG), single photon emission computer tomography (SPECT), and positron emission tomography (PET).
fMRI is a scan that shows neuronal activation during working memory tasks by measuring blood oxygen changes (39). Preliminary data from McGill University have shown significant fMRI reductions in regional brain activation the months after concussion in patients experiencing cognitive postconcussion symptoms. A specific change in fMRI signal also predicted those patients experiencing postconcussion related depression. The preliminary study also has found that fMRI abnormalities improved as patient symptoms improved (39). These studies lend credence to the view that PCS is a physiologic process. If found to be sensitive and specific, fMRI offers exciting possibilities in diagnosing PCS and monitoring for successful treatment of individual patients.
MEG is an electrophysiological diagnostic test that Lewine found was highly specific at diagnosing cognitive problems in preliminary studies. The brain location of slow waves on MEG correlated with each specific cognitive symptom. However, MEG did not detect abnormalities associated with psychiatric and physical symptoms (26).
SPECT is a nuclear imaging modality that reflects blood flow through the brain, and studies have been mixed regarding SPECT's ability to diagnose PCS. Lewine found that basal ganglia hypoperfusion correlated closely with postconcussive headaches, and frontal hypoperfusion on SPECT predicted deficits in executive function (26). Another study regarding the role of PET scanning found that patients with PCS did not have resting state abnormalities, but hypometabolic changes were found during spatial working memory tasks (6).
Recent research has found novel brain proteins, including S100, neuron-specific enolase, and cleaved Tau, that may have a role in diagnosing PCS. These proteins are thought to be released into serum after axonal brain injury and blood-brain barrier disruption. Unfortunately, a recent review of 11 prospective cohort studies found that no biomarker consistently has demonstrated the ability to predict PCS after mTBI (2).
Typical medical management of PCS includes close observation and adjustment of activity. Symptoms often are treated independently by known means, and data on whether these treatments are as effective for postconcussion patients is mixed. McCrory commented in 2002 that there is no evidence-based treatment for the sports medicine physician to offer (30). While little evidence based research concerning the treatment of sports-related PCS has been conducted in the past decade, recent literature regarding non-sports-related head injury suggests some medical options to consider in the treatment of PCS.
When available, patients with PCS should be referred to an experienced neuropsychologist for evaluation. Computerized neuropsychiatric testing may be helpful as a tool for return-to-play decisions, and with persisting symptoms, traditional neuropsychiatric testing can be considered. These tests generally are more sensitive and can detail specific deficits experienced by the athlete. Cognitive rehabilitation can facilitate a return to work or school by helping the patient adjust to his or her individually identified deficits (49).
Medications may be beneficial in some cases. Dopaminergic agents can be considered for treatment of cognitive PCS symptoms. Amantidine, initially introduced as an influenza medication, has positive effects on dopamine levels and activity in the brain, and one small retrospective study showed improved clinical outcomes in patients with brain injury who were treated with doses of 50-400 mg·day−1 (36,41). Levadopa and bromocriptine have been found to have similar beneficial effects in cognition after brain injury (41). Because of similarities in PCS and Alzheimer's memory and attention deficits, treating cholinergic dysfunction has been considered as well. Published reports regarding phyostigmine, CDP-choline, and donepezil have shown some improvement in cognitive performance in PCS patients (49). MEG scanning has shown epileptiform spikes in some patients with PCS despite no history of seizure. In one case, treatment with depakote showed improvement in memory function, although attention and processing speed did not improve (26).
Athletes are unique in their behavioral responses to injury, particularly brain injury (40). Psychiatric counseling should be considered, and the choice of medication for mood symptoms in PCS is controversial. A double-blind, placebo-controlled trial conducted in Korea on patients an average of 30 d after mTBI measured the efficacy of methylphenidate versus sertraline and found that both medications improved the depressive symptoms of PCS, and methylphenidate improved cognition for 4 wk after initiation (25). Another study showed that sertraline was helpful in depression symptoms and improving general cognitive efficiency after mTBI (14). An earlier study on 15 patients with traumatic brain injuries found that long-term benefits of methylphenidate use were not impressive (16). Response to tricyclic medications also has been questioned, with one study showing no improvement in headache or depression with amitriptyline medication in PCS patients (44). However, trazodone has been suggested for treatment of PCS-related insomnia (41). Anecdotal evidence suggests that anxiety symptoms related to PCS be treated with selective serotonin reuptake inhibitors (SSRI), buspirone, or the opioid antagonist, naltrexone; however, benzodiazepines and antipsychotics should be avoided as they worsen cognitive effects of PCS (41).
Medical treatment for the physical symptoms of PCS should begin at low doses with gradual increases as patients with PCS may be particularly sensitive to medication (41). Hecht described that PCS headaches that radiate from the neck can be related to occipital neuralgia, and in a small sample of patients, occipital nerve block was very effective for treating this symptom (18). Further review of the literature found one study on mice showing that dehydroepiandosterone sulfate (DHEAS), sometimes used as a weight lifting supplement, had beneficial effects on cognitive and behavioral symptoms of PCS (34).
The variety of treatments that have been suggested and tried for PCS demonstrates the lack of a clear consensus and the heterogenicity of presentation. The variability of symptoms also may relate to the areas of the brain affected by injury. As there are no large, randomized trials to guide therapy, treatment must be individualized and symptoms treated as they would be in an uninjured patient. An athlete with attentional issues may benefit from stimulants, one with depression may benefit from antidepressants, and one with headaches may respond to medications and therapies typically used to treat headaches. In recalcitrant cases, off-label medication options might be considered. As our understanding of the pathogenesis of PCS evolves, so will our treatment.
FOLLOW-UP AND RETURN TO PLAY
An athlete with PCS should be followed closely by his or her physician and neuropsychologist, and return-to-play decisions should be individualized. There is no evidence-based guideline, but these decisions should follow some of the same general principles used for return to play after concussion.
A trial off of any medications for PCS is essential to be certain the athlete has truly become asymptomatic, and it is prudent to have a symptom-free interval before returning to contact sports. Depending on how long an athlete's PCS symptoms have lasted, consideration should be given as to whether they should return to contact sports at all. If an athlete elects to go back to contact sports, the athlete and his or her family need to have demonstrated a clear understanding of the potential long-term risks involved. There is concern for recurrence of PCS, and there are no data to confirm that one will fully recover from subsequent concussions. Return-to-play decisions in children need to be even more conservative given the unknown developmental effects of concussion and the increased effects of concussion on the immature brain (22).
Return to noncontact aerobic exercise also is debatable. The initial treatment of concussion should include a period of cognitive and physical rest, as not to interfere with the brain's increased metabolic demand acutely after injury. However, as symptoms persist in PCS, athletes can suffer from physical and emotional consequences of inactivity. Leddy proposed that individualized activity plans including submaximal, asymptomatic aerobic exercise are beneficial for patients in improving mood, sleep, and other symptoms of PCS (24). Return to noncontact aerobic activity even can be considered in those individuals taking medications to address their symptoms as long as symptoms do not increase with activity.
Return to nonsport activity is another concern for a treating physician. PCS symptoms greatly can impact one's ability to function in school, work, and family settings. The physician should educate the patient's family about PCS and advocate for the patient to have workplace accommodations and vocational rehabilitation if needed. School-age athletes will need increased time for assignments and tests and extra tutoring. If specialized education becomes necessary, a child may benefit from a Section 504 plan or individualized education program that schools must lawfully administer for children with disabilities (22).
PCS is a frustrating and enigmatic problem for the athlete and for the clinician. There is much to learn. Key points to remember regarding PCS include:
* PCS remains a clinical diagnosis without a consistent definition. In athletes, a prolonged persistence of concussion symptoms is considered PCS.
* The pathophysiology of PCS has been debated. Newer testing methods may offer insight into the true causes of this disease.
* Studies have shown that amnesia, noise and light sensitivity, migraine headache, self-reported cognitive decline, and anxiety soon after concussion may predict PCS. In the general population, women and those with preinjury psychiatric disease have a higher incidence of PCS.
* There are a variety of cognitive, physical, and emotional symptoms seen in PCS.
* CT and MRI are not helpful to diagnose or predict PCS, but newer modalities, especially fMRI, are promising. Serum biomarkers are not proven at this time.
* Medications that address symptoms may be considered in the treatment of PCS. Dosing should begin low and titrated upward slowly.
* Return-to-contact sports only should be considered when a patient is symptom-free.
* Low-intensity aerobic exercise can be considered if it does not recreate or worsen symptoms.
* Patients with PCS may need accommodations at work and school when suffering.
Further research is needed regarding PCS. There are currently five ongoing National Institutes of Health (NIH)-funded research studies regarding PCS, including trials on fMRI, cognitive therapy, and medical treatment options. As our understanding of this difficult condition advances, improved counseling and evidence-based therapeutic options will greatly help our "miserable" patients.
The authors thank Dr. Stan Herring for his help in initiating this project.
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