CHAPTER 1 CONCUSSION MANAGEMENT: WHAT IS OUR ROLE?

(1)

CONCUSSION MANAGEMENT: WHAT IS OUR ROLE?

Felix Meza ^ Douglas Aukerman^ and Wayne Sebastianelli^

^Sport Medicine Center, The Pennsylvania State University, University Drive, University Park, PA, 16802 fmeza@ psu.edu

^Sport Medicine Center, The Pennsylvania State University, University Drive, University Park, PA, 16802; daukerman@psu.edu

^Department of Orthopaedics and Rehabilitation Milton Hershey Medical College, The Pennsylvania State University, University Drive, University Park, PA, 16802;

wsebastinelli @psu. edu

Abstract: In sports such as football, wrestling, and ice hockey, a minor "ding" or mild concussion is often an expected right of passage, or at least an expected injury. Being "in a fog" after a tackle, or a minor headache after a collision, is often considered "no big deal" to most athletes. Master comments that in boxing "being knocked-out is not considered dangerous but just part of the sport", in fact few coaches are aware that this change in mental status is actually a sign of brain injury. (McCrory, 2004) These neurological injuries both in isolation and in series must be taken seriously if we are to protect the athlete. Numerous physicians and clinical researchers have dedicated their lives work to a systematic approach to the early detection and management of concussions.

Although it has taken a few well publicized cases of significant injury and death to bring this issue to the forefront of sports medicine, our basic understanding of concussion management needs to continue to advance.

By educating the medical community on the hazards associated with MTBI, it has also made both athletes and coaches aware that further medical assessment and evaluations should not be put off when an athlete is exhibiting post concussive signs and symptoms. At the most basic level, athletes are being protected from further brain injury by not being allowed to return to play until they are asymptomatic. Ultimately our role is to protect the athlete from further harm.

Keyv^ords: Concussion; Management; Retum-to-play; Case studies.

1. INTRODUCTION

Our basic understanding of concussion or mild traumatic brain injury (MTBI) is rooted in the neurology literature on severe brain injury following motor vehicle accidents or more severe blunt trauma. Much of this literature focuses in on disabling neurological injuries or the comatosed patient. The

(2)

378 Sebastianelli, Meza and Aukerman

Glasgow Coma scale, although useful in severe traumatic injuries, is not practical when discussing the majority of MTBI seen at sporting events. In fact a loss of consciousness or an intracranial hemorrhage is not associated with the majority of cases of concussions (Guskiewicz et al., 2000). This chapter will give a brief review of the literature on MTBI, summarize the most recent guidelines at the time of publishing, discuss future research areas and outline the clinician's role in the management of concussion.

!•!• Epidemiology

Mild traumatic head injury accounts for 75% of all brain injuries (Goetz, 2003) with concussion being the most common sports-related head injury (Cooper et al., 2003). In the United States alone, there are approximately 300,000 sports-related head injuries every year (Centers for Disease Control and Prevention, 1997). The reported incidence of concussion in high school players ranges from 5.6% to as high as 20% (Guskiewicz et al., 2000;

Gerberich, 1983). The incidence of concussion in collegiate football players ranges from 5.6% to 10% (Guskiewicz et al., 2000). This is similar to an NFL reported incidence of 7.9% for NFL quarterbacks (Pellman et al., 2004). Pellman et al., report that during the 1996-2001 seasons on average there were 131.2 +/- 26.8 concussions per year in the NFL (Pellman et al., 2004). Guskiewicz, et.al reported that "high school and collegiate football players who sustain a concussion are nearly three times more likely to sustain a second concussion in the same season than those players that have not" (Guskiewicz et al., 2000). At the NCAA Division I level Guskiewicz et al., reported that of the 246 players that sustained a concussion in their study, 9.8% of them went on to have another injury in the same season (Guskiewicz et al., 2000). As in the case of non-sports related head injuries, a true number of concussion injuries is difficult to come by because of an under-reporting of "dings" or "bell-ringers" by athletes. Attempts are being made to have a more unified reporting system at the collegiate level that might give a more accurate incidence of concussion in college athletics (Dick, 2005). It is our opinion that in addition to under-reporting, the lack of a universally agreed upon definition of concussion has also hindered attempts at accurate epidemiological data.

1.2, Definition of Concussion

Although debate exists as to the true definition of concussion, most authors quote the Committee on Head Injury Nomenclature of the Congress of Neurological Surgeons definition given in 1966: "a clinical syndrome characterized by immediate and transient post-traumatic impairment of neural function, such as alteration of consciousness, disturbance of vision.

(3)

equilibrium, etc, due to brainstem involvement" (Committee on Head Injury, 1966). Many definitions of what a concussion entails have since followed.

The American Academy of Neurology defined concussion as a "trauma- induced alteration in mental status that may or may not involve loss of consciousness" (AAN Summary Statement, 1997). The AOSSM concussion workshop defined concussion as ''any alteration in cerebral function caused by a direct or indirect (rotation) force transmitted to the head resulting in acute signs and symptoms of injury"(Wojtys, 1999). Finally the 2000 Vienna concussion conference defined a concussion as "a complex pathophysiological process affecting the brain, induced by traumatic biomechanical forces" (Aubry et al., 2001).

What is not debated is the importance of early recognition of signs and symptoms in our athletes to prevent further injury. Post-concussion signs and symptoms include: headache, dizziness, irritability, amnesia (either retrograde or anterograde), fatigue, sensitivity to light, sensitivity to noise, insomnia or other sleep disturbances, report of fogginess, difficulty with concentration, depression, anxiety, significant mood changes, poor balance, nausea, and vomiting (Cantu, 2003, McCrory et al., 2005). Although a rare complication, most feared is the possibility of developing second impact syndrome. Second impact syndrome is a rapid onset of cerebral swelling that occurs after a second injury to an already concussed individual. Most commonly seen in children and adolescents, the cerebral swelling can lead to brain stem herniation and death (McCrory, 2002). Often the second injury is minor; however the player's response to this minor injury can be very dramatic.

Cantu describes case reports of adolescent football and rugby players that sustain a second injury and within seconds to minutes "complain of severe headache, tingling in their legs, collapse to the ground, semicomatosed with rapidly dilating pupils, loss of eye movement, and ensuing respiratory failure" (Cantu, 2003). Although the exact pathophysiology is unknown it is thought to involve a loss of vascular auto- regulation in the brain leading to vascular engorgement within the brain and subsequent herniation (Cantu, 2003). Attempts to minimize brain injury with second impact syndrome would include immediate intubation and administration of an osmotic diuretic such as mannitol (Cantu 2003).

However, education of coaches, parents, and athletes in collision sports about the risks associated with too quick a return to activity would seem to be the best preventative measure.

1.3. Pathophysiology of Concussion

Numerous studies have attempted to outline the pathophysiology behind concussion; nonetheless it is still an area of unknowns. Animal models and

(4)

studies of severe brain injuries in humans have been used to extrapolate the human brains response to mild traumatic brain injury. The majority of brain injuries in sports are closed head injuries. Closed head injuries can be divided into focal versus diffuse injury. Focal injuries are a result of a direct mechanical force to the skull, whereas diffuse injuries are a result of acceleration and deceleration forces and rotational sheering forces applied to the brain (Okonkwo, 2003). Focal injuries may lead to epidural or subdural hematoma formation and/or a cerebral coup or contrecoup contusion. "A coup contusion occurs at the site of impact in the absence of a fracture, whereas a contrecoup contusion occurs in the brain opposite the point of impact" (Goetz, 2003). Diffuse injuries or more specifically diffuse axonal injury (DAI) may lead to edema and herniation that may result in coma and ultimately death (Okonkwo, 2003). In both focal and diffuse injury the generation of free radicals or reactive oxygen species (ROS) may contribute to further damage (Okonkwo, 2003). 'Tree radicals generated following trauma cause widespread neuronal damage via peroxidation of lipid membranes and oxidation of cellular proteins and nucleic acids, as well as secondary damage via damage to cerebral microvasculature" (Okonkwo, 2003). Although the exact pathophysiology of MTBI is yet unknown, a concussion could be considered a less severe form of a focal or diffuse injury.

Utilizing rat models, Hovda et al., has attempted to understand the pathophysiology of concussion, and describes a post brain injury metabolic cascade. Following a MTBI there is an intracellular and extracellular shift of sodium, potassium, and calcium ions (Giza & Hovda, 2001). Specifically, after injury there is an increase in extracellular potassium and an increase in intracellular calcium, resulting from the activation of excitatory neurotransmitters such as glutamate and N-methyl-D-aspartate (NMDA) (Giza & Hovda, 2001). This triggers the activation of sodium-potassium pumps and a subsequent increase in the intracellular need for glucose metabolism to drive the pump. During this process Hovda describes a period of "diminished cerebral blood flow" (Giza & Hovda, 2001). What occurs next is a mismatch of increased glucose utilization in the cell and decreased cerebral blood flow, leaving the brain vulnerable to secondary injury mechanisms (Giza & Hovda, 2001). Just how these secondary injury mechanisms function is a topic of extensive research. Okonkwo et al., describes how "High intraneuronal calcium activates numerous secondary injury mechanisms, such as nitric oxide systems, calpains, caspases, calcineurin, endonucleases, and phosphatases" (Okonkwo, 2003). The brains vulnerability to these secondary injury mechanisms and ways to prevent them could prove to be valuable in the management of severe concussions in the future. Finally, the role of lipid peroxidation, mitochondrial damage, and apoptosis in traumatic brain injury are other areas of research.

(5)

2. CONCUSSION GRADING SYSTEMS

Initially developed to provide clear and concise guidelines for both the assessment and subsequent return to play after mild traumatic brain injury, concussion grading scales have since fallen out of favor because of a lack of supporting literature. Below is a summary of the most commonly used grading systems which focused on loss of consciousness (LOC), post- traumatic amnesia (PTA), and post concussion signs and symptoms (PCSS) in order to grade severity of injury and recommendations for return to play.

Cantu first proposed a grading scale for concussion severity and return to play in 1986; he subsequently revised these recommendations in 2001 (Cantu, 1986; Cantu, 2001). Cantu stresses the fact that definitive concussion severity should not be made on the day of injury and in fact should be deferred until all signs and symptoms of concussion have cleared (Cantu Presentation, 2005). The Colorado Medical Society published guidelines in 1991, which focused on the use of loss of consciousness and amnesia as a marker for severity (Colorado Medical Society, 1991). Finally, The American Academy of Neurology published a consensus statement in 1997 which focused on loss of consciousness as a main marker of severity (Quality Standards Subcommittee AAN, 1997). These guidelines are compared in Table 1.

Table J - Comparison of Grading Scales

Cantu - Revised (2001)

American Academy of Neurology (1997)

Colorado Medical Society (1991)

Grade I - Mild No LOC

PTA < 30 minutes PCSS < 30 minutes No LOC

Transient confusion PCSS < 15 minutes No LOC

No PTA PCSS

Grade II - Mod LOC < 1 minute or PTA or PCSS > 30 minutes < 24 hrs No LOC

Transient confusion PCSS> 15 minutes No LOC

PCSS PTA

Grade III - Severe L0C>1 minute PTA > 24 hrs PCSS > 7 days Any LOC

Any LOC

LOG - loss of consciousness, PTA - post-traumatic amnesia, PCSS - post concussion signs and symptoms

Debate exists about use of loss of consciousness as an indicator of severity. Lovell et al. performed neuropsychological testing on patients with and without loss of consciousness admitted to a trauma service and found that LOC did not result in greater neuropsychological impairment (Lovell, 1999). These results then lead to questions regarding the importance of LOC as a marker for concussion severity and subsequent return to play.

Guskiewicz et al., reported only 8.9% of all 888 players that sustained a

(6)

382 SebastianelU, Meza and Aukerman

concussion had an associated loss of consciousness (Guskiewicz et al., 2000). In addition, the use of amnesia as a marker for concussion severity has also been questioned (Cantu, 2001).

Concussion grading scales are not currently recommended as guidelines for concussion management from either the 2000 Vienna or 2004 Prague concussion conferences because of a lack of validating literature. Instead the Prague conference recommends individually guided determination of injury severity and subsequent return to play decision making (McCrory et al., 2005). A new classification system was proposed at the Prague conference.

It was suggested that the severity of a concussion could only be determined after all signs and symptoms had resolved (McCrory et al., 2005). For management purposes, it was recommended to classify a concussion as either simple or complex. A simple concussion was defined as an 'injury that progressively resolves without complications over 7-10 days" (McCrory et al., 2005). A complex concussion was defined as "any concussion with persistent symptoms, prolonged loss of consciousness greater than one minute, prolonged cognitive impairment following injury, or individuals who have suffered multiple concussions." (McCrory et al., 2005) Essentially, all Grade I concussions and the majority of Grade II concussions under the Cantu guidelines would fall under the category of a simple concussion. Prolonged Grade II injuries and Grade III injuries would be classified as complex.

2.I. Return to play guidelines based on grading scales

Return to activity recommendations for a first time concussion, are summarized below in Table 2.

Table 2. Recommendations for Return to Play-First concussion

Cantu ~ Revised (2001)

American Academy of Neurology (1997) Colorado Medical Society (1991)

Grade I One week

Same day if PCSS resolve < 15 min Same day if PCSS resolves < 20 min

Grade II One week One week

One week

Grade III One month Two weeks

One month

PCSS - post concussion signs and symptoms

Same day return to play for Grade I "dings" has been advocated by all grading scales except under the revised Cantu, with the assumption that quick resolution of signs and symptoms correlated with cerebral recovery.

(7)

Recent studies have questioned this assumption. Lovell studied 84 high school football players with reported Grade I concussions and found that the majority had deficits on neuropsychological testing up to 7 days out from time of injury (Lovell, 2004). All three guidelines agree that Grade II concussions warrant a minimum of one week out from activity prior to return to play, but controversy persists on length of time out of activity for Grade III concussions. As mentioned previously, the likelihood of a second concussion within the same season is at least three times greater (Guskiewicz et al., 2000). Cantu advocates a minimum of two weeks out of activity for a second Grade I concussion within a season and a minimum of one month out of activity for a second Grade II concussion within a season (Cantu, 2001). Cantu recommends termination of a season if more than three Grade I or Grade II concussions in a season (Cantu, 2001). However the most important cornerstone of all concussion management guidelines is that an athlete can not return to activity if they are symptomatic. According to the 2004 Prague guidelines, all simple concussions would warrant a return to activity in a stepwise fashion once the player becomes asymptomatic, with a minimum of 5 days prior to full return to competition (McCrory et al., 2005). Complex concussions should be evaluated on a case-by-case basis by a qualified physician (McCrory et al., 2005).

2*2. Role of imaging in concussion management

At the Vienna conference it was recognized that post-concussion neuroimaging, such as CT and MRI are usually normal (Aubry et al., 2002).

Although there are no clear guidelines of when to obtain neuroimaging studies after a concussion, the Prague guidelines recommend consideration of neuroimaging if there is a prolonged duration of symptoms, development of worsening post-concussive symptoms, or a focal neurological deficit that might indicate an intra-cerebral hematoma or other structural lesion (McCrory et al., 2005). Current research is being conducted on the validity of PET scans, SPECT scans, or functional MRI modalities for post- concussion assessment (Chen, 2004). On going studies are also looking at the role of EEG in post-concussion evaluation (Slobounov et al., 2005).

2,3. Neuropsychological testing

Neuropsychological testing has continued to be endorsed as a corner stone of concussion management (McCrory et al., 2005). Numerous studies have been published over the past ten years attempting to solidify its role in post-concussion management. Echemendia states that "data from neuropsychological testing provides the clinician with an objective index of cognitive functioning that can signal the return to pre-injury levels of

(8)

functioning" (Echemendia et al., 2001). Although matched control baselines exist, it is most useful to have the athlete perform patient specific baseline testing prior to an injury. Currently the Prague conference does not endorse the use of neuropsychological testing in simple concussions, but does recommend its use in complex concussions (McCrory et al., 2005).

Ultimately the clinician must decide how best to utilize neuropsychological testing as a tool for return to play decision-making.

2.4. Medical/Ethical issues

What we do not know is how many concussions are too many? It is clear that the repetitive damage provoked by boxing can lead to dementia pugilistica, but how many concussions an adolescent brain can withstand versus an adult brain is still unknown. Field et al., suggests that there are differences in recovery times between high school age and college age athletes (Field et al., 2003). One of the hardest decisions a team physician has to make is when to medically disqualify an athlete because of multiple concussions. Cantu recommends absolute contraindications for return to competition should include; any evidence of neurological deficit, persistent post concussion signs and symptoms at rest, neuropsychological testing below baseline, and CT or MRI evidence of a significant cerebral lesion (Cantu, 2003). Relative contraindications would include prolonged post concussion symptoms and significant post concussion symptoms with a minor injury (Cantu, 2003). Without clear guidelines for exclusion these decisions must be made in conjunction with the athlete and by clinicians with experience in concussion management.

3. INTERESTING CONCUSSION CASES

Although athletes suffering from concussions frequently report similar symptoms, every concussion is unique even when it occurs within the same individual. On the continuum of head injuries, from mild insult to severe brain trauma, each case can present with a diverse grouping of signs and symptoms. Every physician covering athletic events has treated athletes with unwitnessed head trauma and the ensuing myriad of subtle symptoms that complicate concussion diagnosis and treatment. When caring for athletes, medical personnel should exercise a high degree of suspicion, because even mild concussions may have long term sequelae. This section will present several sports related concussion cases with interesting details that will hopefully provoke thought, discussion, and debate.

(9)

3.1. Case 1

A 16 year old high school linebacker, who has no history of previous concussion or head trauma, runs over to the sideline during the end of the second quarter. He jogs over to the athletic trainer with tears streaming from his face. Known as a hard hitter and the strongest physical player on the team, he has never sought help from the medical team. His only complaint tonight is that he can not stop crying and has no idea why he is doing so. He denies any pain or injury as well as any emotional or psychological stressors at home. He also denies having conflict with any coach or teammate over his play that game. He reports that all he remembers is hitting the running back early in the first quarter to end the drive on a goal line stand.

Retrospectively, he also notes that he had some difficulty in making the play call and adjustments during the second quarter. He denies any headache, or other symptom suggestive of a concussion. Upon exam, the player has normal SAC and denies any symptom increase with activity. He has intact memory and recall. The player was removed from the game despite his adamant protest. His coach also was angered and verbally pressured the trainer to return his all-state linebacker to the game. The athlete's parents came down from the stands and also stated matter-of-factly to the medical team that their son was fine and needed to play. Despite this pressure, the medical team stood fast to the decision to remove the athlete from the game.

The following day, the athlete's parents took him to his pediatrician, who cleared the athlete because "his symptoms were improving" and recommended that he ease back into things over the next 3 to 4 days. The reason given for the pediatrician's recommendation was that this is the way he did things. Despite the pediatrician's recommendations, the team physician referred the football player for formal neuropsychological testing, the results of which showed major declines in visual speed processing. The athlete also reported a headache following the testing procedure. He was monitored over the course of the next several days, and his emotional state and all other symptoms returned to baseline. He then had an unremarkable exercise challenge. After missing the next seven days of practice and a game, he returned to the season and had no further sequelae.

3.2. Case 2

A 21 year old female presents for evaluation of a headache with physical activity. She is a rugby athlete, who reports that her headache began after a collision in a scrum four days earlier. She reports that she does not recall the incident other than she was not allowed back to play by the athletic trainer.

She noted that she had dizziness, nausea, and photophobia present for 30 hours after the incident. She reports that she has had previous head injuries

(10)

as well, indicating that this is her fifth concussion in the past 2 years of rugby. All of the concussions have been minor and associated with a headache and visual problems for a few days. However, each time she returned back to practice and did not tell anybody. She had recurrent injury on three consecutive days in practice three weeks prior to this incident but did not report these as well. Since that time, she has had a headache, dizziness, and nausea that have progressed in severity leading up to this most recent injury. She states now that she has head pain any time she has any type of physical activity and has worsening headache and mild dizziness.

She has difficulty concentrating, still has emotional outbursts, and still has periods of amnesia. These worsen with activity.

She also recalls that four years ago she had evaluation for headaches by her primary care physician and her hometown emergency department following a fall where she hit her head, that included an MRI of her brain.

She was told she had a "structural abnormality" that needed to be followed but she was afraid to do so and has had no further evaluation. She has had a history of headaches with extreme activity over the past decade of her life.

The athlete was held from all activity and formal neuropsychological testing was performed. She also had a repeat MRI performed given her history, which revealed an Arnold Chiari Malformation (the cerebellar tonsils protruding out of the foramen magnum). The athlete was disqualified from further contact sports at that point. She ultimately has had a surgical decompression by neurosurgical specialists and resolution of her symptoms.

3.3. Case 3: Concussion with overlying depression

The 22 year old football player was stuck in the side of the helmet during the first period of a football game. He reports that initially he did not think he was hurt, but began experiencing difficulty reading plays that were delivered from the sideline. He was subsequently removed due to the concern of a concussion. Immediately following removal from the game, he developed several complaints including visual disturbance, feeling in a fog, mild headache and problems with attention. These symptoms persisted for 2 hours. At 48 hours he reports trouble falling asleep, sadness and nervousness. At time of neuropsychological testing, he had deficits in immediate and delayed visual and verbal memory. In addition he had difficulty with speeded visual attention and cognitive flexibility. He also reported a mild level of depression on a depression scale. He did not have a previous history of depression. One week later, all of his symptoms had resolved, as had his neuropsychological testing but he continued to have abnormalities on the depression scale.

(11)

3A. Summary

Each of these cases has something unique to offer. Symptoms can vary from psychological disturbances to cognitive dysfunction. Under reporting by the patient is common and must be factored into the assessment. The apparent mechanism of trauma may not accurately reflect the severity of injury. Finally, the threshold for concussion is lowered with each successive brain injury.

CONCLUSIONS

Because of the large number of at risk individuals in athletics, the discussion and management of concussion has become a multi-disciplinary topic. Welcoming input and management recommendations from fields such as Neurology, Sports Medicine, Orthopaedics, Neuropsychology, and Athletic Training, the management of concussion has continued to evolve.

At one time based solely on empirically driven guidelines, recent clinical research and literature has challenged these guidelines and opened the door for new standards of care in concussion management. With the pressure of quick return to competition from players, coaches, and even parents, evidence based guidelines can be utilized as a clear reference to support decisions to keep athletes out from competitions that might put them at harm. Often athletic trainers at all levels of experience are the first to assess individuals with concussions and without clear guidelines the best decision may not be made. The goal now is to develop evidence based guidelines to assist numerous athletic trainers and physicians to make an accurate assessment and develop a safe and reasonable return to play criteria. The exciting aspect of concussion management is that new research continues to bring a better understanding of the pathophysiology behind MTBI. By educating the medical community on the hazards associated with MTBI, it has also made both athletes and coaches aware that further medical assessment and evaluations should not be put off when an athlete is exhibiting post concussive signs and symptoms. At the most basic level, athletes are being protected from further brain injury by not being allowed to return to play until they are asymptomatic. Ultimately our role is to protect the athlete from further harm.

REFERENCES

McCrory, P., Matser, E. et al.(2004). Sports neurology. The Lancet Neurology, 3, 435-440.

Guskiewicz, K.,Weaver, N. et al. (2000). Epidemiology of concussion in collegiate and high school football players American Journal of Sports Medicine, 28, 643-650.

Pellman, E. et al. (2994). Concussion in professional football: Epidemiological features of game injuries and review of the literature. Neurosurgery, 3, 54:81-96.

(12)

Goetz, C. (2003). Textbook of clinical neurology, 2"'^ ed, pp. 1129-1135. Philadelphia:

Saunders.

Cooper, M., McGee, K., & Anderson, D. (2003). Epidemiology of athletic head and neck injuries. Clinical Sports Medicine, 22, 427-443.

Centers for Disease Control and Prevention, Sports-related recurrent brain injuries - United States. (1997). MMWR, 46(10), 224-227.

Gerberich, S., et al. (1983). Concussion incidences and severity in secondary school varsity football players. American Journal Public Health, 73, 1370-1375.

Dick, R. (2005). NCAA Updates. AMSSM Annual Meeting April 19'^ 2005 Austin, Texas.

Committee on Head Injury: Nomenclature of the Congress of Neurological Surgeons:

Glossary of head injury including some definitions of injury to the cervical spine. (1996).

Clinical Neurosurgery, 12, 386-394.

Quality Standards Subcommittee, American Academy of Neurology. Practice parameter: the management of concussion in sports (summary statement). (1997). Neurology, 48, 581- 585.

Wojtys, E., Hovda, D., et al.(1999). Concussion in sports. American Journal of Sports Medicine, 27, 676-687.

Aubry, M., Cantu, R., Dvorak, J. et al. (2001). Summary and Agreement Statement of the first International Conference on Concussion in Sport, Vienna 2001. Clinical Journal of Sport Medicine, 12,6-12.

Cantu, R. (2003). Recurrent athletic head injury: risks and when to retire Clinical Sports Medicine, 22, 593-603.

McCrory, P., & Johnston, K. (2002). Acute clinical symptoms of concussion. Physician Sports Medicine, 30, 8.

Okonkwo, D., & J. Stone, J. (2003). Basic science of closed head injuries and spinal cord injuries Clinical Sports Medicine, 22, 467-481.

Giza, C & Hovda, D. (2001). The neurometabolic cascade of concussion. Journal of Athletic Training, 36(3), 228-235.

Cantu, R. (1986). Guidelines for return to contact sports after a cerebral concussion. Physical Sports Medicine, 14,75-83.

Cantu, R. (2001). Posttraumatic retrograde and anterograde amnesia. Journal of Athletic Training, 36(3), 244-248.

Cantu, R. (2005). Concussion in athletics: Ongoing controversy. Penn State University Conference April 29-30, 2005. State College, PA.

Colorado Medical Society, Guidelines for the management of concussion in sports. Review, May 1991. Denver: Colorado Medical Society.

Lovell, M, et al., (1999). Does loss of consciousness predict neuropsychological decrements SifiQY concussionl Clinical Journal of Sport Medicine, 9, 193-198.

McCrory, P., Johnston, K., et al. (2005). Summary and Agreement Statement of the 2"^

International Conference on Concussion in Sport, Prague. Clinical Journal of Sport Medicine, 75,48-55.

Lovell, M., & Collins, M. (2004). Grade one or "Ding" concussions in high school athletes.

American Journal of Sports Medicine, 32(1), 123-133.

Lovell, M., Collins, M., & Bradley, J. (2004). Return to play following sports- related concussion. Clinical Sports Medicine, 23, 421-441.

Chen, J., Johnston, K. et al. (2004). Functional abnormalities in symptomatic concussed athletes: an fMRI study. Neuroimage, 22, 68-82

Slobounov, S., Sebastianelli, W., & Moose, R. (2005). Alteration of posture-related cortical potentials in mild traumatic brain injury Neuroscience Letters, 383(3), 251-255.

Echemendia, R., Putukian, M., et al. (2001). Neuropsychological test performance prior to and following sports-related mild traumatic brain injury. Clinical Journal of Sports Medicine, 77, 23-31.

(13)

Echemendia, R., & Cantu, R. (2004). Traumatic Brain Injury in Sports, pp. 479-498.

Netherlands: Taylor and Francis.

Field, M. et al. (2003). Does age play a role in recovery from sports-related concussion? A comparison of high school and collegiate athletes. Journal of Pediatrics, 142, 546-553.