Sports Concussion and the Clinical Neurologist, Part I

Transcription

1 Sports Concussion and the Clinical Neurologist, Part I Neurologists, who increasingly will confront patients diagnosed with sports concussion, must be adept at identifying and managing the condition. Part I of a series reviews epidemiology, definition, mechanism, and clinical manifestations. By Francis X. Conidi, DO, MS On the surface, efforts to reduce concussions in professional football would not seem controversial. And those who would benefit the most from a less hazardous workplace the players may be expected to be the ones most supportive of a rule change designed to decrease bonecrushing hits. But when the National Football League (NFL) announced a rule change to their kickoff format that would decrease action for the sake of player safety, players reacted negatively. "I think the NFL is destroying the true game of football and the physicality that America has grown to love, former player Donnie Nickey is reported as saying. "It's an injustice to the game and the men who have made their living covering kickoffs and sacrificing their bodies to have their jobs made obsolete." The NFL moved the kickoff spot up five yards (from the 30- to the 35-yard line) this season to decrease head injuries by increasing touchbacks when the ball sails out of the end zone or deep enough to render the kick unreturnable. Ironically, this recent action reverses a 1994 rule that moved the kickoff to the 30-yard line to decrease the number of touchbacks and bring more excitement to the game. There are an estimated 1.6 to 3.8 million sports related concussions annually. 1 However, this number is likely higher, as many athletes fail to report their symptoms for fear that they will not be allowed to return to play. 1,2 Over the past few years the management of sports related concussion has come under considerable scrutiny in the media and public realm, which has led to a Congressional investigation, significant changes in the way the NFL and other professional sports organizations deal with concussion, and most importantly a greater public awareness of the disorder. So while there is a good deal of resistance from the professional athletes (and fans, for that matter), momentum is picking up for increased safety, at least through government and governing bodies. Furthermore, 29 states now have passed sports concussion laws, with 14 states with pending legislation. Thankfully a majority of the laws require an athlete be cleared by a trained physician prior to returning to play. Concussion is and will always be a neurological disorder. It is therefore imperative that all neurologists have at least a basic understanding of all aspects of sports concussion as they are likely going to be called upon to evaluate these athletes, especially the more refractory cases. 40 Practical Neurology September/October 2011

2 Epidemiology Sports Related Concussion, when bicycle associated accidents are included, is the most common cause of head trauma in children under 18, and the second most common cause in adults after motor vehicle accidents. 3-5 Approximately 60 percent of male high school football players and 40 percent of women high school soccer players will suffer a concussion Concussion is and will always be a neurological disorder. It is therefore imperative that all neurologists have at least a basic understanding of all aspects of sports concussion as they are likely going to be called upon to evaluate these athletes, especially the more refractory cases. during their high school career. 6,7 In fact, more than 60,000 high school athletes participating in sports such as ice hockey, football, lacrosse, soccer, and cheerleading suffer concussions each year. 6-8 More troubling is almost half of these athletes returned to play prematurely, setting them up for further injury and even death, 7,9-11 with five out of every seven deaths from football related injuries deemed secondary to head trauma (National Center for Catastrophic Injury Research; 2009). In all amateur sports, ice hockey has the highest rate of concussion amongst males, followed by football then boxing/taekwondo. 12 At the college level the numbers are not much better, with an estimated annual concussion rate of 3.02 concussions per 1,000 plays in football players. 7 Perhaps more alarming is that football is second to men s ice hockey in percentage of players who suffer concussion. 7,13 Finally, for all sports, women s ice hockey has the highest concussion rate, with one study estimating an incidence of approximately 22 percent in NCAA players. 13 Definition At present there is no uniform accepted definition of sports related concussion. Sports Related Concussion and Mild Traumatic Brain injury (MTBI) are often used synonymously. The Consensus Statement on Concussion in Sport, i.e. Zurich 2008, felt that there was a difference between concussion and MTBI, however the publication did not attempt to define MTBI. 14 The outdated American Academy of Neurology practice parameter defines concussion as, a trauma-induced alteration in mental status that may or not involve a loss of consciousness. Confusion and amnesia are the hallmarks of concussion. The confusion may occur immediately after the blow to the head, or several minutes later. 15 Zurich defines sports concussion as, a complex pathophysiological process affecting the brain, induced by traumatic biomechanical forces. It lists several common features that incorporate clinical, pathologic, and biomechanical injury constructs that may be utilized in defining the nature of the concussion or head injury, including features listed in Table A better way to define concussion may be in relation to the mechanism, i.e. sports, falls, motor vehicle, or blast. In addition, taking into account the underlying physiology, biomechanical process, and symptoms may be more practical especially when it comes to designing research studies. Using these parameters, the definition of sports concussion is a prolonged transient alteration in neuronal function caused by a blow to the athlete s head and/or body with transmission of force to the head, resulting in rotational and/or translational (i.e. angular and lateral) movement of the head resulting in neurological September/October 2011 Practical Neurology 41

3 symptoms that resolve sequentially over time. A lack of a standard definition creates significant issues when attempting to conduct research studies, develop guidelines, pass legislation, and evaluate devices and equipment used to diagnose, treat and prevent sports related concussion. Mechanism There are several theories as to the possible mechanism of sports concussion, however none are universally accepted. 14,17 It is hypothesized that the characteristics needed to sustain a concussion include rotational, angular, and/or lateral forces causing rotation of the cerebral hemispheres around the upper brainstem. 14 A direct blow to the head is not required. The mechanism is felt to be similar to what is seen in falls and motor vehicle accidents, however different from blast injuries suffered by our military heroes which involve primary, secondary and tertiary components A number of studies have attempted to identify possible biomechanical mechanisms Headshots or helmet hits were the most common mechanism; shots to the lower side of the helmet and oblique portion of the face mask 23 induce translational and rotational forces on the head. Blindside hits to the body, which can induce lateral flexion of the neck and rotation of the head, have also been demonstrated to induce concussion. 23 In addition to the acute effects of high impact collisions, there also appear to be chronic effects of repeated lower impact collisions, such as those experienced by offensive and defensive lineman, which are hypothesized to be involved in early memory impairment that is now being seen in these individuals. 24 The NFL has found that concussion in professional football players involves a mean impact velocity of 9.3 meters/sec or 20.8 mph. In comparison, if a car hits a pillar or structure the impact duration is less than 6 meters/sec. 23 Definition of Sports Concussion A prolonged transient alteration in neuronal function caused by a blow to the athlete s head and/or body with transmission of force to the head, resulting in rotational and/or translational (i.e., angular and lateral) movement of the head resulting in neurological symptoms that resolve sequentially over time. Neuroanatomy Simulated game studies by the NFL to test which brain structures were most affected in concussion have demonstrated "hot spots" in the temporal lobe adjacent to the impact, which migrate to the far temporal lobe after head acceleration. The fornix, midbrain, and corpus callosum experienced late strain. Midbrain strain correlated with memory and cognitive problems and removal from play after concussion, whereas dizziness correlated with early strain in the orbital-frontal cortex and temporal lobe. 25 Functional MRI (fmri) has also been used to study athletes with sports related concussion. Deficits were found in the parietal cortex, right dorsolateral prefrontal cortex, and right hippocampus. 26 The above structures play a role in attention, arousal, sleep, memory, dizziness, reaction time, and headache. Table 1. Some Features of Sports Concussion 16 Concussion may be caused by a direct blow to the head, face, neck or elsewhere on the body with an implosive force transmitted to the head. - Concussion typically results in the rapid onset of short-lived impairment of neurological function that resolves spontaneously. - Concussion may result in neuropathological changes, but the acute clinical symptoms largely reflect a functional disturbance rather that a structural injury. - Concussion results in a graded set of clinical symptoms that may or may not involve loss of consciousness. Resolution of the clinical and cognitive symptoms typically follows a sequential course; however it is important to note that in a small percentage of cases, post concussive symptoms may be prolonged. No abnormality is seen on standard structural neuroimaging studies. 42 Practical Neurology September/October 2011

4 Table 2. AAN Sports Neurology Position Statement 1. Any athlete suspected of suffering a concussion should be removed from participation until evaluated by a physician. 2. No athlete should be allowed to participate in sports if they are still experiencing symptoms of a concussion. 3. Following a concussion a physician, preferably a neurologist, should be consulted prior to clearing the athlete to return to participation. 4. A certified coach or athletic trainer should be present at all sporting events, including practices, where risk of concussion is involved. 5. Education efforts should be maximized to improve the understanding of concussion by all athletes, parents, and coaches. 6. An athlete must be completely asymptomatic (cognitively/ physically), off of any concussion related medications) and complete a graded protocol prior to RTP. Note: This is an updated version of the original released in Point #6 has since been added. Pathophysiology It is essential that the neurologist have a detailed understanding of the pathophysiology of sports related concussion. Understanding the pathophysiology is key when considering an athlete returning to play (RTP) and for the development of true evidenced based RTP guidelines. At present what is known is based on rat percussion models (Giza and others) and a few neuroimaging studies. There are three phases of concussion: the acute, intermediate, and late phases. Post-concussive deficits are based on temporary neuronal dysfunction and not cell death. The acute phase is characterized by metabolic and ion derangements, disruption of neural membranes, and axonal stretching. The latter results in abrupt and indiscriminant release of neurotransmitters and unchecked ion fluxes. Excitatory neurotransmitters, such as NMDA and glutamate, trigger neuronal depolarization with an efflux of potassium and influx of calcium. Increased extracellular calcium triggers further neuronal depolarization and further release of excitatory neurotransmitters and still further release of potassium into the extracellular space. Normally excessive extracellular calcium is taken up by surrounding glial cells, however this mechanism is overcome in concussion. The massive excitation is followed by a wave of neuronal suppression (i.e., Spreading Depression). 27,28 Early LOC, amnesia and other cognitive deficits may be a result of posttraumatic Spreading Depression. Membrane pumps become activated in an effort to restore homeostasis, which results in increased glucose utilization. Increased glycolysis leads to increased lactate production which results in neuronal dysfunction through processes such as metabolic acidosis, membrane damage, alterations in blood brain barrier permeability, and cerebral edema. The intermediate phase is characterized by uncoupling of glucose metabolism and cerebral blood flow. Calcium influx, mitochondrial dysfunction and delayed glucose hypometabolism also occur. 27,28 Uncoupling causes a 50 percent reduction of blood flow that creates an energy mismatch. 27,28 There is a biphasic recovery of oxidative metabolism with a reduction on day 1, recovery by day 2, bottom out by day 5, and complete recovery by day ,28 Calcium accumulation can persist for two to four days, and the excess calcium is sequestered in mitochondria resulting in impaired metabolism and energy failure. 27,28 Cerebral glucose use is diminished by 24 hours and can last up to two to four weeks post-injury with the average recovery at 10 days. Cerebral glucose metabolism and oxidative metabolism correlate with the average concussion recovery time of 10 days. 27,28 Intracellular magnesium levels are immediately reduced and remain so for up to four days, and magnesium level recovery is correlated with improvement in motor function. 27,28 The hallmarks of the late phase are delayed cell death, persistent calcium accumulation, and neurotransmitter alteration. 27,28 Persistent elevations in intracellular calcium can lead to over activation of enzymes and free radical production resulting in cell death. 27,28 Postconcussion alterations in NMDA, adrenergic, cholinergic, and GABA neurotransmission can result in long-term deficits in memory and cogni- September/October 2011 Practical Neurology 43

5 tion, even in the setting of minimal anatomic damage. 27 Loss of forebrain cholinergic neurons can lead to learning and spatial memory deficits. 27 Loss of GABA can result in disinhibition of hippocampal structures (i.e. easy distractibility) and increase the risk of seizures. 27 Repeat concussions during the post injury period, when the cell is most vulnerable, can have catastrophic consequences. In the first 30 minutes when the system is stretched to its maximum, the brain may be unable to respond to a second stimulusinduced increase in cerebral glucose metabolism. 27 An increase in intracellular calcium after a second physiological stimulus can lead to protease activation and programmed cell death. 27 Alterations in NMDA receptor composition can persist for one week post-injury and a second injury in this period can lead to further impairment of excitatory neurotransmission. 27 In summary, concussion is followed by a complex cascade of events that is somewhat analogous to what happened to New Orleans with Hurricane Katrina. When Katrina hit there was an initial blow that resulted in a storm surge and the build-up of massive amounts of water in Lake Pontchartrain and the subsequent give way of the levies (the immediate phase). This was followed by a turning on of pumps and patching of the levies (the intermediate phase). Even once the water was pumped out and the rebuilding began, the city was never quite the same (the late phase). What would have happened if another hurricane hit New Orleans within a few days, weeks, or even in the first few months before the city had a chance to completely fix the levies and rebuild its structures? The results would have been catastrophic and depending on how soon, the city may never have recovered. The same is true with a concussed athlete if he or she is allowed to RTP too soon and sustains another concussion. Signs and Symptoms The signs and symptoms of concussion are directly related to the disruption of brain physiology. As a rule, the longer the symptoms last the more severe the concussion. 29 Understanding the signs and symptoms and when they occur is essential in managing Table 3. Stages of Chronic traumatic encephalopathy (CTE) Stage Signs and Symptoms Loss of affect and mild psychosis. Social instability, erratic behavior, memory loss, and mild Parkinsonism. General cognitive dysfunction progressing to dementia, full-blown Parkinsonism, speech and gait abnormalities, dysarthria, dysphagia, and ocular abnormalities/ptosis. the concussed athlete. Immediate signs and symptoms include: vacant stare (befuddled facial expression), delayed verbal and motor responses (slow to answer questions or follow instructions), confusion and inability to focus attention, disorientation (walking in the wrong direction; unaware of time, date, and place), slurred or incoherent speech, gross observable decrease in coordination (stumbling, trouble with tandem gait), emotions out of proportion to circumstances, memory deficits (exhibited by the athlete repeatedly asking the same question that has already been answered or inability to memorize and recall three of three words or three of three objects in five minutes), or any period of loss of consciousness. 14,15 It should be noted that loss of consciousness is not a common symptom, occurring in less than 10 percent of all athletes. 14 Within the first few hours the athlete may experience intermediate symptoms of headache, dizziness, loss of equilibrium or vertigo, lack of awareness of their surroundings and nausea or vomiting. 14,15 As the concussion progresses, late signs and symptoms develop and can include: persistent low grade and sometimes even severe headache (may include photo/phono phobia); light-headedness; poor attention, concentration, and memory; heat intolerance; easy fatigability; sleep disturbances; irritability, anxiety, and/or depressed mood, which are often unrecognized; sleep disturbances; and decreased reaction time and balance which, are the last symptoms to resolve. 14,15 Conclusion Sports related concussion continues to be the most widely publicized neurological disorder. As a result, 44 Practical Neurology September/October 2011

6 neurologists are currently, and even more so in the future going to play a significant role in the management of concussed athletes. It is therefore imperative that they master all facets of the disorder, i.e., from epidemiology to return to play. However, there is still no uniform definition of sports concussion, and very few evidence-based studies outline the duration and prevalence of symptoms. Understanding the physiology over time at the human level is arguably the biggest challenge facing Sports Neurology, and as we will see in the next issue, understanding the brain s physiology will allow for the development of evidenced-based diagnostic testing, treatment and RTP guidelines. Part II of this series, to appear in the November/ December edition, will address diagnosis/testing and treatment. Visit PracticalNeurology.net to download the entire two-part article. Dr. Conidi is the Director of the Florida Center for Headache and Sports Neurology, the team Neurologist for the NHL's Florida Panthers and is an Assistant Clinical Professor of Neurology at Florida State University College of Medicine. He has been elected to serve on the American Academy of Neurology's Sports Neurology Executive Committee and is a consultant for the FDA's Center for Devices and Radiological Health (CDRH), which deals specifically with sports concussion. Please direct any questions and comments to fxneuro@bellsouth.net. 1. Langlois JA, Rutland-Brown W, Wald MM. The epidemiology and impact of traumatic brain injury: a brief overview. The Journal of head trauma rehabilitation 2006;21: McCrea M, Hammeke T, Olsen G, Leo P, Guskiewicz K. Unreported concussion in high school football players: implications for prevention. Clinical journal of sport medicine : official journal of the Canadian Academy of Sport Medicine 2004;14: Kraus JF, Nourjah P. The epidemiology of mild, uncomplicated brain injury. The Journal of trauma 1988;28: Luerssen TG, Klauber MR, Marshall LF. Outcome from head injury related to patient's age. A longitudinal prospective study of adult and pediatric head injury. Journal of neurosurgery 1988;68: Lescohier I, DiScala C. Blunt trauma in children: causes and outcomes of head versus extracranial injury. Pediatrics 1993;91: Lincoln AE, Caswell SV, Almquist JL, Dunn RE, Norris JB, Hinton RY. Trends in concussion incidence in high school sports: a prospective 11-year study. The American journal of sports medicine 2011;39: Daneshvar DH, Nowinski CJ, McKee AC, Cantu RC. The epidemiology of sport-related concussion. Clinics in sports medicine 2011;30:1-17, vii. 8. Schulz MR, Marshall SW, Mueller FO, et al. Incidence and risk factors for concussion in high school athletes, North Carolina, American journal of epidemiology 2004;160: Yard EE, Comstock RD. Compliance with return to play guidelines following concussion in US high school athletes, Brain injury : [BI] 2009;23: Putukian M, Aubry M, McCrory P. Return to play after sports concussion in elite and non-elite athletes? British journal of sports medicine 2009;43 Suppl 1:i Mayers L. Return-to-play criteria after athletic concussion: a need for revision. Archives of neurology 2008;65: Koh JO, Cassidy JD, Watkinson EJ. Incidence of concussion in contact sports: a systematic review of the evidence. Brain injury : [BI] 2003;17: Hootman JM, Dick R, Agel J. Epidemiology of collegiate injuries for 15 sports: summary and recommendations for injury prevention initiatives. Journal of athletic training 2007;42: McCrory P, Meeuwisse W, Johnston K, et al. Consensus statement on concussion in sport - The 3rd international conference on concussion in sport held in Zurich, November PM & R : the journal of injury, function, and rehabilitation 2009;1: Practice parameter: the management of concussion in sports (summary statement). Report of the Quality Standards Subcommittee. Neurology 1997;48: McCrory P, Meeuwisse W, Johnston K, et al. Consensus statement on concussion in sport: the 3rd International Conference on Concussion in Sport held in Zurich, November Journal of athletic training 2009;44: Scott Delaney J, Puni V, Rouah F. Mechanisms of injury for concussions in university football, ice hockey, and soccer: a pilot study. Clin J Sport Med 2006;16: Wilk JE, Thomas JL, McGurk DM, Riviere LA, Castro CA, Hoge CW. Mild traumatic brain injury (concussion) during combat: lack of association of blast mechanism with persistent postconcussive symptoms. The Journal of head trauma rehabilitation 2010;25: Belanger HG, Proctor-Weber Z, Kretzmer T, Kim M, French LM, Vanderploeg RD. Symptom complaints following reports of blast versus non-blast mild TBI: does mechanism of injury matter? Clin Neuropsychol 2011;25: Courtney AC, Courtney MW. A thoracic mechanism of mild traumatic brain injury due to blast pressure waves. Med Hypotheses 2009;72: Hinton-Bayre AD, Geffen G, Friis P. Presentation and mechanisms of concussion in professional Rugby League Football. Journal of science and medicine in sport / Sports Medicine Australia 2004;7: Hamberger A, Viano DC, Saljo A, Bolouri H. Concussion in professional football: morphology of brain injuries in the NFL concussion model--part 16. Neurosurgery 2009;64: ; discussion Pellman EJ, Viano DC. Concussion in professional football: summary of the research conducted by the National Football League's Committee on Mild Traumatic Brain Injury. Neurosurgical focus 2006;21:E Prins ML, Hales A, Reger M, Giza CC, Hovda DA. Repeat traumatic brain injury in the juvenile rat is associated with increased axonal injury and cognitive impairments. Developmental neuroscience 2010;32: Viano DC, Casson IR, Pellman EJ, Zhang L, King AI, Yang KH. Concussion in professional football: brain responses by finite element analysis: part 9. Neurosurgery 2005;57: ; discussion Keightley M, Green S, Reed N, Agnihotri S, Wilkinson A, Lobaugh N. An investigation of the effects of sports-related concussion in youth using functional magnetic resonance imaging and the head impact telemetry system. Journal of visualized experiments : JoVE Barkhoudarian G, Hovda DA, Giza CC. The molecular pathophysiology of concussive brain injury. Clinics in sports medicine 2011;30:33-48, vii-iii. 28. Giza CC, Hovda DA. The Neurometabolic Cascade of Concussion. Journal of athletic training 2001;36: Makdissi M, Darby D, Maruff P, Ugoni A, Brukner P, McCrory PR. Natural history of concussion in sport: markers of severity and implications for management. The American journal of sports medicine 2010;38: September/October 2011 Practical Neurology 45