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The difficult concussion patient: what is the bestapproach to investigation and management ofpersistent (>10 days) postconcussive symptoms? Michael Makdissi,1,2 Robert C Cantu,3 Karen M Johnston,4 Paul McCrory,1Willem H Meeuwisse5 Persistent symptoms following concussion are a cause Background Concussion in sport typically recovers of significant morbidity and frustration to the athlete clinically within 10 days of injury. In some cases, and pose a management challenge to the clinician.
however, symptoms may be prolonged or complications While there has been an explosion of studies on the may develop. The objectives of the current paper are to acute management of concussion over the past review the literature regarding the difficult concussion decade, data on the management of prolonged recov- and to provide recommendations for an approach to the investigation and management of patients with approach to the difficult concussion is largely based on anecdotal evidence or extrapolation from studies Methods A qualitative review of the literature on on moderate-to-severe traumatic brain injury (TBI).
and Sports Medicine, Universityof Melbourne, Melbourne, concussion in sport was conducted with a focus on The objectives of the current study were to prolonged recovery, long-term complications and review the literature regarding the difficult concus- management including investigation and treatment sion and to provide recommendations for an strategies. MEDLINE and Sports Discus databases were approach to the investigation and management of Results Persistent symptoms (>10 days) are generally reported in 10–15% of concussions. This figure may be higher in certain sports (eg, ice hockey) and populations (eg, children). In general, symptoms are not specific to PubMed) and SportDiscus databases were under- of Kinesiology and HotchkissBrain Institute, University concussion and it is important to consider and manage taken using the key words ‘concussion’, ‘mild trau- coexistent pathologies. Investigations may include formal matic brain injury’, ‘head injury’ and ‘sport’ or neuropsychological testing and conventional ‘athlete/athletic’. These terms were combined with neuroimaging to exclude structural pathology. Currently, the following keywords to identify the literature for there is insufficient evidence to recommend routine difficult concussions and key aspects of investiga- clinical use of advanced neuroimaging techniques or tion and management: ‘symptoms’, ‘complex’, ‘dif- genetics markers. Preliminary studies demonstrate the ficult’, ‘prolonged’, ‘persistent’, ‘post-concussion potential benefit of subsymptom threshold activity as syndrome’, ‘investigation’, ‘imaging’, ‘biomarker’, part of a comprehensive rehabilitation programme.
‘gene/genetic’, ‘treatment’, ‘medication’, ‘manage- Burgundy St HeidelbergAustralia, Heidelberg, VIC Limited research is available on pharmacological ment’, ‘exercise’ and ‘rehabilitation’.
The search was limited to the English language Conclusions Cases of concussion in sport where and focused on original papers published in the clinical recovery falls outside the expected window past 10 years. Reference lists from retrieved articles Received 26 January 2013Accepted 29 January 2013 (ie, 10 days) should be managed in a multidisciplinary were searched for additional articles, and the manner by healthcare providers with experience in authors’ own collections of articles were included sports-related concussion. Important components of management, after the initial period of physical andcognitive rest, include associated therapies such as cognitive, vestibular, physical and psychological therapy, assessment for other causes of prolonged symptoms and Concussion typically results in a range of symptoms consideration of a graded exercise programme at a level and signs in a number of different domains.1–3 The clinical features vary, but commonly reported symp-toms include headache, nausea, dizziness andbalance Over the past decade, recommendations for the man- fatigue.4–9 Prospective cohort studies and system- agement of concussion in sport have centred on phys- atic reviews have consistently demonstrated that the ical and cognitive rest until symptoms resolve and majority of cases of concussion in adult populations then a graded programme of exertion prior to resolve within 10 days of injury.6 9–12 A ‘difficult medical clearance and return to play.1–3 This basic concussion’ can be described as one in which clin- approach works well for the majority of concussions ical recovery falls outside the expected window (ie, where clinical features resolve progressively within 10 days. In a number of cases, however, recovery can The incidence of prolonged clinical recovery fol- lowing concussion varies depending on the cohort Makdissi M, et al. Br J Sports Med 2013;47:308–313. doi:10.1136/bjsports-2013-092255 Summary of studies reporting symptoms at baseline Mean total symptom score (±SD): males: 7.3 Fatigue, headache, sleep disturbance, difficulty Mean total symptom score (±SD): males 4.6 Fatigue/low-energy, drowsiness, neck pain, difficulty Fatigue, drowsiness, headache, trouble falling asleep, No significant differences between males andfemales (range 0–108)No significant difference between males andfemales Fatigue, trouble falling asleep, difficulty concentrating, No significant differences between males and HIS, Head Injury Scale (9 items, 7-point Likert scale); NR, not reported; PCS, Postconcussion Symptom Scale; SCAT, Sport Concussion Assessment Tool.
being investigated (as well as the time frame used to define ‘pro- (eg, depression, anxiety, etc) have been used in the study of longed’). Studies have shown that approximately 10–15% of retired players.35 36 Given the complex nature of postconcussion collegiate and professional American football players have symp- symptoms, similar questionnaires may also be beneficial in the toms beyond 10 days.7 10 13 Similar figures have been demon- assessment of difficult concussions. Domains that should be con- strated in Australian football.4 9 Higher rates of prolonged recovery (ie, over 30% of cases) have been reported following ▸ Depression and anxiety (eg, Hospital Anxiety and concussion in ice hockey,6 and in cohorts of high school Depression Scale, Beck Depression Inventory, Depression Anxiety Stress Scale, Profile of Moods States); Common persistent symptoms include headache, depression, ▸ Headache and migraine (Headache Impact Test, Migraine ‘difficulty concentrating’, ‘fatigue or low energy’, ‘difficulty sleeping’ or ‘feeling not quiet right, in a fog or slowed ▸ General health and disability (eg, Short-form 36 Health down’.4 7 9 10 13 16 These symptoms are non-specific and may Survey Questionnaire, Health-Related Quality of Life); be reported in healthy athletic populations at baseline (table 1) ▸ Sleep (eg, Medical Outcomes Study Sleep Scale Survey); and in patients with other injuries, illnesses or neuropsychiatric ▸ Drug and alcohol use/abuse (eg, Drug Abuse Screening conditions. These same symptoms have also been reported in Test, Alcohol Use Disorders Identification Test).
general trauma patients, individuals with anxiety or depression, The advantages of a more detailed, semiquantitative assess- patients with chronic pain syndromes, soldiers with combat ment are that it may help identify other causes or contributing stress and individuals who are involved in litigation regardless factors to the individual’s symptoms and may facilitate monitor- ing over time. While specific patient-reported outcome measures When assessing postconcussion symptoms, it is important to have yet to be validated in concussion, they may serve as useful consider that reporting of symptoms may be affected by a clinical and research assessment tools.
number of factors including sex, socioeconomic factors, concur-rent illness or musculoskeletal injury and moderate-to-high intensity exercise.18 26–29 Studies in patients with mild TBI have The assessment of recovery following concussion is currently also demonstrated that symptom reporting can be influenced by limited by the absence of simple and reliable direct measures of general health status,30 other medical conditions such as brain function. Instead, clinicians must rely on indirect measures migraines31 and psychological factors such as coexisting anxiety to inform clinical judgement, such as the symptoms and signs of concussion (including neurological and balance assessments), in The method used for symptom reporting can also impact on addition to the use of brief neuropsychological tests to estimate the results. For example, Krol and Mrazik33 performed a cross- sectional study in 117 athletes comparing self-reported symp-toms to symptoms endorsed during an interview. The authorsfound a higher number of symptoms reported and a greater overall symptom score in the self-administered condition.33 Computerised screening neuropsychological test batteries have They also found that athletes reported more symptoms when become an important component of concussion assessment.1–3 the interviewer was woman.33 Similarly, Iverson et al34 demon- The test batteries have been shown to be sensitive to changes in strated a higher reporting of symptoms on a self-administered cognitive function following concussion. Moreover, they have questionnaire when compared with a structured interview in a been shown to detect cognitive deficits in a significant propor- tion of individuals even after the symptoms have resolved.9 37 General health questionnaires that incorporate patient- Although formal neuropsychological testing is also recom- mended in cases of concussion with persistent symptoms, there Makdissi M, et al. Br J Sports Med 2013;47:308–313. doi:10.1136/bjsports-2013-092255 is no literature on the test properties (sensitivity, specificity, pre- concussion. It requires further consideration outside of the dictive value, etc) in this setting.
Advanced imaging and investigation techniques Advanced imaging and investigation techniques have demon- strated changes in brain function, activation patterns and white The current treatment approach for difficult concussions is matter fibre tracts in cases of concussion with prolonged symp- based largely on an extension of the guidelines for acute injuries toms (table 2A). Often, these changes exist even when the (ie, rest until symptoms resolve, followed by the use of com- athlete has recovered clinically and returned to sport (table 2B).
bined clinical measures of recovery to determine the timing of As such, the significance of these changes remains unclear at this return to play). While an initial brief period of rest may be time. Nevertheless, advanced imaging and investigation techni- important in the management of acute concussion, there is ques (such as Diffusion Tensor Imaging, functional MRI, MR limited evidence that further rest is beneficial in cases where spectroscopy, quantitative EEG, etc) may hold hope for future assessment protocols in concussion. In the short term, their use Conversely, preliminary evidence suggests that an active in the research setting should continue to be encouraged.
rehabilitation programme is useful for the management of con-cussion where the symptoms are prolonged (table 3). Therehabilitation programme is started even in the presence of Preliminary research reveals a potential association between gen- The graded exercise test has also been demonstrated to have good inter-rater and test–retest reliability.44 Apolipoprotein E (APOE) has been the most extensively studied When dizziness or disequilibrium is a prominent feature of per- gene in TBI. Jordan et al38 demonstrated a relationship between sistent symptoms following concussion, vestibular rehabilitation APOE4 genotype and chronic TBI score, particularly in high may be useful.45 In a cohort of individuals with blast-related mild exposure boxers (ie, more than 12 professional bouts). Similarly, TBI, Gottshall and colleagues demonstrated improvement in Kutner et al39 studied the potential influence of APOE4 geno- symptoms after an 8-week period of vestibular physiotherapy.46 type in a cohort of 53 active professional American footballers Other treatments have been used anecdotally for the manage- and found that players with at least one copy of the APOE4 ment of specific symptoms. For example, manual or physical allele scored lower on tests of attention and information pro- therapy may be used to treat myofascial pain or neck trigger cessing speed and accuracy. In a neuropathological study of ath- points contributing to headaches; cognitive therapy including letes with Chronic Traumatic Encephalopathy (CTE), an memory tasks as well as learning coping skills may be useful for increased frequency of the APOE4 allele was noted among cases some patients with persistent cognitive symptoms; and those of pathologically confirmed CTE.40 Recently, however, a large who have problems with anxiety, panic attacks or other psycho- case series did not find a definite relationship between the logical or emotional problems may benefit from meditation, bio- APOE genotype and CTE, especially in lesser grades of CTE.41 feedback or psychological therapy. At present, however, there Other genes that have been considered include the APOE pro- are limited data on these techniques in the management of pro- moter and Tau, with no consistent findings regarding an affect longed symptoms following concussion.
on outcome following concussion in sport.
Despite the methodological limitations of these studies, they provide preliminary evidence of a complex inter-relationship Numerous medications are available to treat the range of symp- between head injury, genetics and the risk of cumulative damage.
toms that are observed following concussion.47 Many of these However, more research is required in this area before genetic medications have been investigated in patients with moderate or testing can be recommended as part of the clinical work-up of severe TBI, but there are few trials that have been conducted in In a small cohort of volunteers diagnosed with major depres- Management of structural injuries masquerading as sion following mild TBI, Fann et al48 demonstrated an improve- ment in symptoms and function with the use of sertraline.
Any athlete that sustains a head injury is at risk of having a In a recent retrospective study, Reddy et al49 examined the structural brain injury (eg, brain contusion). One of the critical effects of amantadine in 25 adolescent athletes with postconcus- roles of the initial medical assessment is to examine the player sion symptoms that persisted longer than 21 days. Individuals neurologically for such injuries. There are well described and were compared with historical controls, and all individuals were validated guidelines for the use of imaging in the acute stage fol- assessed using a computerised neurocognitive test battery. The lowing head injury (eg, the Canadian CT head Rule or the New authors showed that the group treated with 100 mg of amanta- Orleans Criteria).42 43 Furthermore, in athletes with persistent dine twice per day demonstrated greater improvements in their symptoms or cognitive deficits, consideration should be given to reaction time, verbal memory and symptom reporting.49 conventional neuroimaging to investigate for an underlying A number of different antimigraine treatments have been assessed in small studies of patients with headaches following mild To date, there are no published studies evaluating treatment TBI (table 4). The studies all report moderate to good results, but strategies in athletes who sustain structural head injuries.
the findings have not been confirmed in larger randomised control Consequently, decisions regarding their management, including trials, and nor have they been trialled specifically in patients with return to play, should be made by a clinician experienced in persistent symptoms following concussion in sport.
structural brain injury and based on the type of injury (eg, frac-ture and haemorrhage), relative risks associated with return to Components of a comprehensive concussion clinic sport and the presence of ongoing sequelae (eg, symptoms, Current consensus advocates a multifaceted clinical approach to signs, cognitive deficits). Structural brain injury is not a the assessment of concussion. This is perhaps even more Makdissi M, et al. Br J Sports Med 2013;47:308–313. doi:10.1136/bjsports-2013-092255 Changes observed on advanced imaging and investigation techniques A. Athletes with persistent symptoms following concussion Significantly reduced task-related BOLD changes in the prefrontal cortex in athletes with prolonged symptoms following concussion Activation patterns improved as symptoms improved on follow-up Significant increase in MD in concussed individuals Similar results were observed in the moderate but not severe TBI patients 14 Patients with mild TBI—recruited from 2 Attenuated BOLD signal changes and reduced amplitude for the working memory task were observed in the mild TBI group BOLD signal changes were correlated with symptom severity MT (measured using navigated transcranial MT was higher in some (but not all) mild TBI individuals compared to Changes were observed even in individuals who had recovered clinically The results suggest that subtle prolonged changes may exist in some patients following mTBI and that in a proportion of these patients thechanges may be ‘compensated’ B. Athletes with concussion whose symptoms had resolved Self-reported symptoms recovered within 3–15 days Used single voxel (ROI: right frontal lobe), Significant differences between concussed and control groups were observed in metabolite ratios at day 3 postinjury. Metabolite changes gradually recovered to control levels within 30 days of injury Neurometabolic differences between concussed and control groups were observed in the acute phase (lower N-acetylaspartate:creatine levels in the prefrontal cortex and lower glutamate:creatine levels in the motor cortex)as well as the delayed phase (increase in the myoinositol levels in the rsFMRI (ROI: right dorsolateral prefrontal All concussion individuals were asymptomatic at rest and had no NP rsFMRI revealed disrupted functional network both at rest and in response Concussed athletes had lower P3b amplitudes than the control athletes Adolescent athletes showed persistent deficits in working memory Significant default mode network connectivity differences were observed Regression analysis revealed a significant reduction in magnitude of connection between various structures in the brain as a function of thenumber of concussions BOLD, blood oxygenation level-dependent; ERP, event-related brain potential; FA, fractional anisotropy; fMRI, functional magnetic resonance imaging; NP, neuropsychological; MD, mean diffusivity; MRS, MR spectroscopy; MT, motor threshold; ROI,regions of interest; rsFMRI, resting state fMRI; TBI, traumatic brain injury.
(beginning with submaximal aerobic training that is, 15 min on a treadmill or stationary bike, then introducing sports-specific training drills for10 min)Found a significant increase in exercise toleranceand reduction in symptom score (30.0±20.8 atpresentation to 6.7±5.7 at discharge)Mean duration of intervention 4.4±2.6 weeks Exercise at an intensity of 80% of the maximum heart rate achieved on the treadmill test before reported being symptom-free at restAthletes recovered faster than non-athletesRate of symptom improvement was directlyrelated to exercise intensity achieved 41/57 Who completed the exercise programme important in the setting of prolonged symptoms, where the diagnosis is not always clear (ie, there are other causes of pro- A ‘difficult concussion’ can be described as one in which clinical longed symptoms) or when superimposed factors lead to a recovery falls outside the expected window (ie, 10 days in the pattern of deterioration rather than the expected improvement.
Some components of a comprehensive concussion clinic aresummarised in table 5, although the list is by no means com-plete and expands with time and experience. For instance,access to expertise such as sport psychology, physiatry, psych- iatry, occupational therapy, social work and educational consul- Persistent symptoms are non-specific and may be caused by or tants are now included in such a list. In addition, in the setting contributed to by other conditions (such as migraine, mental of the difficult concussion, access to appropriate rehabilitation health issues, concurrent injuries, etc). The assessment of per- strategies, both physical and cognitive, is important and identifi- sistent symptoms therefore requires a careful history (including cation of programme leadership and coordination is key.
both past and family history) and examination (including assess- Community resources may be incorporated in addition to ment of the cervical spine and vestibular function). The current postconcussion symptom checklist on the SCAT2 alone is insuf- Ideally, the concussion clinic would also have a central role in ficient for the assessment of persistent symptoms, without a athlete and public education and health advocacy participating detailed history of the symptoms. The addition of patient- in collaborative efforts. Access to academic studies, as well as reported outcome measures to the assessment battery in pro- participating in and benefiting from research findings, helps to longed or difficult cases (especially in the case of the retired nurture the future directions of such a programme and benefits player with ongoing cognitive issues) would provide a more the injured athlete. The physical and administrative structure comprehensive, quantifiable approach to assessment and may and support to the programme will facilitate excellence in the allow identification of other causes or contributing factors to Pharmacotherapy for persistent post-traumatic headache ‘Dramatic reduction’ in the frequency and severity of Reported a good-to-excellent response in 29 of 34 patients.
Also noted improvement in memory symptoms, sleep 60% Reported mild-to-moderate improvement after 1 month of treatment. The remaining 40% either showed no response (26%) or stopped treatment because of side effects Makdissi M, et al. Br J Sports Med 2013;47:308–313. doi:10.1136/bjsports-2013-092255 severe symptoms at rest that preclude the start of a graded Components of a comprehensive concussion clinic rehabilitation programme. Medications generally should be restricted to the management of related syndromes (eg,migraine, sleep disturbance, etc).
Difficult concussions should be managed in a multidisciplin- ary manner. Ideally, this is in the setting of a concussion clinic with access to expertise in a wide range of areas.
Contributors MM, RCC, KMJ, PMC and WHM all made substantial contributions to conception and design, acquisition and interpretation of data; drafting and final approval of the version to be published.
Competing interests See the supplementary online data for competing interests (
Provenance and peer review Commissioned; internally peer reviewed.
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Packard RC. Treatment of chronic daily posttraumatic headache with divalproex Makdissi M, et al. Br J Sports Med 2013;47:308–313. doi:10.1136/bjsports-2013-092255 The difficult concussion patient: what is the
best approach to investigation and

management of persistent (>10
postconcussive symptoms?

Michael Makdissi, Robert C Cantu, Karen M Johnston, et al.
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