neuroimaging of sports concussions...sports concussions teresa g odle, ba, els i n 2004, university...

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Neuroimaging of Sports ConcussionsTeresa G Odle, BA, ELS

In 2004, University of North Carolina researchers mounted sensors on foot-ball helmets and determined that some collisions during football

games are similar in intensity to an auto-mobile hitting a wall at 25 mph.1 These collisions can result in a concussion, a transient disturbance in brain function caused by trauma.2 An estimated 1.6 million to 3.8 million sports concussions occur each year in the United States.3

In the past, concussions also have been called mild traumatic brain injuries (mTBIs). Most recent recom-mendations reported that people with concussions usually fully recover, but because mTBI can cause persistent symptoms, the 2 terms are not syn-onymous.3 Concussions are a subset of mTBI, but not all mTBIs are concus-sions.2 Another reason the terms are not synonymous is that mTBIs exist along a TBI severity spectrum, causing a pathological injury to the extent that

damage is perceived on neuroimaging. In contrast, concussions show symp-toms of functional disturbances that do not appear on computed tomography (CT) or magnetic resonance (MR) imaging examinations. Despite the benign findings, concussion can lead to long-term effects, some severe.4

Patients with symptoms of concus-sion can have significant pathology that is difficult to diagnose.5 Evidence shows potential long-term functional and psy-chiatric complications after concussion in adult athletes.6 Sports concussions are unique in that athletes return to the same setting that put them at risk for initial concussion; often, they return to the sport too soon. A study of 170 patients in an Ontario, Canada, practice reported that in 43.5% of cases, patients who had received a sports concussion returned to play too soon.7 As a result, sports concussions can have more serious con-sequences than apparent from a single

After completing this article, the reader should be able to:�� Discuss sports concussion incidence and reasons for increased attention to these injuries in children and adults.�� Describe the biomechanics of concussion and common signs and symptoms.�� List long-term complications and late sequelae from sports concussions.�� Articulate the related laws, programs, and initiatives aimed at decreasing sports concussion occurrence and effects.�� Discuss treatment recommendations for sports concussion.�� Explain the role of conventional and advanced imaging in diagnosis, management, and research of sports concussions.

Concussions resulting from sports activities have received attention in recent years, and failure to prevent head injury has undergone scrutiny. Although many factors contribute to sports concussion incidence, determining when an athlete can return to play is crucial to minimizing long-term effects of concussion. To date, neuroimaging plays a limited role in concussion evaluation, but conventional and advanced neuroimaging techniques are contributing to the body of research on their future use in evaluation.

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Neuroimaging of Sports Concussions

Changes to cerebral blood f low can cause symp-toms such as migraine headaches. When axons are involved (particularly following acceleration from impact), diffuse white matter lesions arise. The effects of the multifocal lesions vary based on the brain regions injured. Focal damage to axonal cyto-skeletons occurs and, combined with loss of elasticity, can cause breakage of microtubules, preventing the tubules from realigning. Inf lammation can promote demyelination of axons. The role of inf lammation in axonal regeneration is uncertain but might be linked to later neurodegenerative disease following brain injury.3

The 2 primary forces that lead to concussions are direct impact to the head and deceleration or accel-eration forces. A forceful direct blow causes direct injury at the point of contact and is called a coup injury. Direct injury typically is represented by contusions.5,14 Examples of direct force sports injuries include instances such as a baseball strike to the head, head-to-head colli-sions, and the head striking the floor.15

Acceleration and deceleration lead to shear forces and both tensile and compressive strain on tissue; the forces typically are represented as contrecoup injuries, which affect the contralateral side of the brain from forcing the brain against the skull. The forces damage the brain’s white matter by causing diffuse axonal and vascular injury from stretching.5,14 At times, an injury involves combined coup-contrecoup mechanisms, lead-ing to damage to the impacted side of the brain and the opposite side as the brain lags immediately following acceleration.16

Sports injury biomechanics vary from 1 sport or type of injury to another. Compression of the head causes injury at the point of contact, but tensile forces can lead to contrecoup injury.14,17 The brain can more easily endure a brief, compressive force than it can ten-sion and shearing forces.16 A violent impact can lead to shearing injury of white matter fibers. In some cases, an athlete is injured by both direct and rotational forces.14,17 In general, the forces lead to a cascading injury of neurometabolism that involves ionic, metabolic, and pathophysiological effects.2

Biomechanics of concussion affect men and women differently. The kinetics involved in head strikes vary

mild head injury.4 Studies have shown a link between number of head impacts and impaired cognition, even within a single sporting season.8

The long-term implications of sports concussion, and particularly of repeat concussions, has increased interest in studying and treating these injuries.9 Most notably, concerns about long-term sequelae from repeat concussions and returning to play too soon have led to increased public attention, programmatic and guide-line recommendations, and regulations.10 Addressing sports concussions is difficult, considering the culture of sports, sideline assessment, and the financial stakes in professional sports.11 Research on long-term implica-tions of concussions continues, and advanced medical imaging plays an important role in the study of sports concussion and possibly in prevention, diagnosis, and treatment efforts.12,13

Mechanisms of Injury and BiomechanicsStudies of the pathophysiology of concussion show

that a complex series of events takes place in the brain.3 Acute functional problems following a concussion arise mostly from the primary brain injury and the neuro-metabolic events that follow, often called a secondary brain injury.11 The primary and secondary injuries inter-act, because the primary injury triggers the subsequent processes.5

Biomechanics of concussion are similar to those of all TBI.5 Mechanical injury from a force disrupts cel-lular membranes, releasing a stream of intracellular potassium. The depolarizing (switch in charges) effects on neurons lead to a loop that causes additional potas-sium and adds to neuronal effects. Neurotransmittters (amino acids) are released in the form of glutamate, which stimulates receptors and further exacerbates the potassium release. Activation of proteases and mitochondrial impairment are among other meta-bolic results of unchecked neurotransmitter release. Following the excitatory cascade, neuronal depression occurs in diffuse areas of the brain. In severe trauma, cells struggle to maintain metabolic balance and acti-vate the lactic acid glycolysis, which accumulates in the brain. The accumulation eventually causes acidosis and breaks down the blood-brain barrier, which can cause cerebral edema.3


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chain of chemical and other responses that can cause malignant cerebral edema without hematoma, hernia-tion, and death.4,9,21

A second blow to the head after a prior concussion that has not subsided fully can lead to neurometabolic imbalances with severe long-term consequences.11 At times, these second injuries lead to diffuse cerebral swelling, severe functional impairment, and death. This reinjury is sometimes called second impact syndrome9; however, labeling a second concussion as a syndrome is controversial and lacks evidence. Still, physicians rec-ognize the serious clinical condition of diffuse cerebral swelling as an important factor in treating concussions and clearing athletes to return to play.4

Some evidence has shown that having a mutation in the calcium channel, voltage dependent, P/Q type, alpha 1A subunit (CACNA1A) gene that is related to encoding of calcium channels could lead to delayed cerebral edema following minor head trauma.21 Researchers continue to discuss the importance of recognizing diffuse cerebral swelling and especially of developing markers to help physicians determine when cerebral recovery takes place following a first concus-sion to better prevent complications and long-term sequelae from a second blow to the head. Few human studies have been completed, and none have identified the precise time after which a second concussion does less damage.4

Repetitive Head TraumaResearch demonstrates increased risks for more

severe neurological effects from repeated concussions and potentially catastrophic long-term consequen-ces.11,19 Repeated mild blows to the head from sports such as soccer can trigger pathological white matter changes in the brain (see Figure 1). Some athletes appear to be more susceptible to long-term effects from repetitive blows than others, although the reasons are not entirely understood.11

With repeated head trauma, athletes face higher risk of developing mild cognitive impairment or demen-tia, depression, and suicidal thoughts or actions.19 Investigators have confirmed that sustained trauma from boxing can lead to progressive neurological dete-rioration, such as dementia.5

between the sexes. Men have larger heads, which can lower acceleration of the head on impact. Women have 43% less mass in their heads and necks than men, and 23% less neck girth. Women’s head-neck segments also are less stiff than men’s (by about 29%) and have 59% less isometric strength. Still, studies relating kinetics to physical differences between the sexes are not con-clusive, likely because of the variables involved (eg, use of head protection, type and velocity of force) and the complex nature of concussion injuries and pathophysi-ology. Studies of the role of hormones in sex-related differences of concussion effects suggest that estrogen could be involved in the brain’s reaction to trauma, but results across studies are not consistent.9

The term concussion can be used to describe the distinct pathophysiological entity or a group of symp-toms that appear following some types of TBI18 and as a separate designation from the term mTBI.3 No defined biomechanical threshold exists for clinical concussion.2 For the purposes of this article, concus-sion refers to a clinical syndrome represented by altered brain memory and orientation function, and sometimes loss of consciousness. The syndrome is caused by biomechanical-induced changes in the brain.18

Second ImpactOne of the greatest concerns following a sports

concussion is susceptibility to another concussion.8 Athletes who have had a concussion are at higher risk for future concussions, and in general, athletes in many sports are at higher risk of head trauma.19 A prior concussion increases the risk for another concus-sion as much as 3-fold to 6-fold.20 Sustaining a second, albeit minor, impact while still experiencing effects and symptoms of a first concussion is particularly troublesome.9,19

Athletes’ reaction times, balance, and cognition usually are impaired following concussion, which places them at higher risk for a second injury and even a severe injury.21 Typically, more significant injuries occur because the first concussion was not recognized or diagnosed or because an athlete returned to play too soon, typically within a month.21,22 If the brain is still in recovery from a first injury, it is vulnerable metaboli-cally to lesser impacts. This vulnerability leads to a


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school students are involved in interscholastic athletics every year in the United States.25 Marar et al studied more than 14 000 sports injuries that were reported for high school athletes between 2008 and 2010.24 Of these injuries, 1289 were concussions occurring in sports competition, and 647 were concussions occurring dur-ing athletic practice.24

Safe Kids Worldwide examined emergency depart-ment data from 2011 to 2012 for sports injuries in children aged 6 to 19 years.26 The group found that 12% of all sports injuries presenting for emergency care in the age group were concussions. Most sports concussions occur in high school athletes, but reports of concussions in younger athletes are increasing.26 In children younger than 10 years, mTBI accounts for 16% of medical visits, and as many as 25% to 50% of all con-cussions in children are from sports injuries.27

FootballFootball is associated with more traumatic brain

injuries than any sport, because of the high contact involved and because more people participate in foot-ball than in other sports in the United States.23 Between 1965 and 1974, at least 167 people died from football-related brain injuries. Since that time, new rules, penalties, and helmet-safety standards have reduced the number of severe TBIs. The emphasis now has shifted to preventing milder TBIs such as concussions.25

At least 10% of college football players and 20% of high school football players have brain injuries each season.4 The Marar et al study found that nearly half (47.1%) of the concussions reported in high school athletes for a 2-year period were from football inju-ries.24 Multiple concussions were noted in nearly 35% of athletes in an early study (1996 to 1997) of high school football players. Most of these injuries were from running plays that led to contact between players. At least 62% of concussions reported in the Marar et al study were a result of tackling.24 A study of NFL player concussions found that causes vary, but that helmet-to-body impacts led to slightly more concussions than helmet-to-helmet contacts.25

Studies suggest a statistically significant increase in concussions when athletes play football at the collegiate level. This could be the result of better access to sports

EpidemiologyAs many as 20% of athletes participating in contact

sports have a concussion each competitive season.4 Estimates of the millions of sports concussions per year vary because of a widespread lack of reporting.2 As many as half of all concussions from sports injuries might never be reported to physicians.2 Multiple factors affect reporting, including failure of some coaches, ath-letic trainers, and other sports medicine professionals to follow concussion assessment and management guide-lines.23 Intense pressure can be placed on athletes and team medical or coaching staffs to keep top perform-ers in play or return them to play as soon as possible. Likewise, players worry about adverse consequences of reporting concussion, particularly at professional levels.4

Although National Football League (NFL) injuries have received more of the spotlight, concussions occur in many sports and affect recreational and athletic par-ticipants at almost all ages.23,24 More than 7 million high

Figure 1. Repeated head trauma effects. Diffuse decrease in fractional anisotropy following remote concussions. Sagittal (A, B), coronal (C, D), and axial (E, F) slices of the tract-based spatial statistics (TBSS) group contrast on fractional anisotropy maps (controls , concussed; red). The contrasts are overlaid on the mean fractional anisotropy skeleton (in green) and the standard MNI152 T1 1-mm brain tem-plate. The results are thresholded at P 5 .05, corrected for multiple comparisons. L 5 left. Reprinted with permission from Tremblay S, Henry LC, Bedetti C, et al. Diffuse white matter tract abnormalities in clinically normal ageing retired athletes with a history of sports-related concussions. Brain. 2014;137(Pt11):3002.

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B D F


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a pitched ball in baseball.23 Marar et al found that 25% of concussions in high school baseball and softball play-ers were the result of fielding a hit ball.24 According to Safe Kids Worldwide, of 61 510 baseball injuries in 2011 among children aged 12 to 17 years, 11% were concus-sions. Of nearly 39 100 softball injuries in the same group, 11% were concussions.30

BasketballBasketball is among the most popular high school and

college sports for both sexes. The sport is associated with higher rates of concussion in female players than in male players.2,23 The Safe Kids Worldwide evaluation of sports injuries in athletes aged 6 to 19 years from 2011 to 2012 found that concussions accounted for 11.5% of basketball injuries in girls and 7.2% in boys.26 Women have more concussions in competitive play than do men, although concussion rates during practice are similar for men and women. Ball handling and chasing of loose balls tend to cause the most concussions in basketball.23 Marar et al found that male high school players had more concussions while shooting or from player-to-player contact than did female athletes.24

WrestlingFewer athletes participate in competitive wrestling,

but the sport is associated with the highest number of injuries among winter high school and college sports. Takedown maneuvers are the most common cause of concussion in the sport, mostly from contact with an opponent, and about one-fourth of the time from head contact with the playing surface.23 Competitive matches were associated with 3 times as many concussions than practice sessions in Marar et al’s study on high school sports concussions. The authors also found that take-down maneuvers accounted for the most concussions among study participants during competitions, with a slightly higher rate of concussions occurring from player-to-surface contact.24

Other SportsConcussions occur in a variety of sports, with injury

levels relating to participation, activities that increase risk of injury, and effectiveness of following rules and wearing protective gear to prevent concussion. According to Safe

medicine professionals and more consistent reporting of the injuries than at the high school level.23 Football also is popular among youths; more than 2.1 million chil-dren aged 6 to 14 years played tackle football in 2015.28 Although head and neck injuries are less common in youth football than other injuries (eg, knee, ankle, hand, and back), the sport can result in severe TBI and concussion along with cumulative effects of repetitive concussions.29

SoccerCompetitive soccer has grown in popularity in the

United States since the 1980s.23 Soccer concussions are among the most prevalent in American organized sports for male and female athletes.2 Concussions often occur in both sexes from head-to-head collisions with other players or from heading the ball.23 A Safe Kids Worldwide evaluation of emergency department visits for sports injuries in athletes aged 6 to 19 years reported that 17.1% of sports injuries seen in girls from soccer were concussions; 12.4% of boys’ injuries were concus-sions.26

In the Marar et al study, high school girls had more soccer concussions than did boys. The study reported that player-to-player impacts caused slightly more con-cussions in boys, whereas girls were injured more from impacts with the soccer ball and falls (impact of play-ing surface).24 Other studies, however, have shown that player contact causes more soccer concussions in both high school and college soccer athletes.2

Baseball and SoftballBaseball and softball players have similar concussion

rates at the high school level, although rates vary based on under-reporting. In general, the literature has shown a rate of 0.03 to 0.08 concussions per 1000 athletes in college baseball games and practices, and 0.04 to 0.09 concussions among college softball players. Still, con-cussions represent a higher percentage of all injuries in softball than in baseball.23 This is evidenced by higher concussion rates among high school softball players than high school baseball players in the Marar et al study.24

Slightly different methods of play (such as pitching speed and mechanisms) lead to more head injuries from


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Many of these symptoms are apparent following all types of TBI, however. For example, headache, cogni-tive impairment, and sleep disturbance are among symptoms common across the TBI severity spectrum. Further, the complex nature of the brain and small degrees in variations in protective gear or of impact force, direction, and other biomechanical factors means that symptoms do not necessarily match the apparent severity of a given injury. Seemingly minor injuries can have lasting effects.5

Estimates show that as many as 47% of athletes report feeling no symptoms after a concussive blow to the head.32 Although concussion effects and symptoms vary from 1 individual to another, the symptoms tend to evolve and appear in phases, and other symptoms might not be apparent until minutes or hours following injury.4,9 Immediate symptoms appear on impact; acute symptoms are evident within hours or days of injury, and subacute symptoms appear up to 4 weeks following injury. Common symptoms of concussion can overlap phases depending on the individual but typically reflect functional disturbances.4 In addition, many symptoms

Kids, ice hockey has fewer overall injuries (9540) than other sports, but 31% of those injuries are concussions. See Table 1 for summaries of concussions in other sports.2,23,24

Signs and SymptomsConcussion leads to neuropathological changes, but

the symptoms reflect functional problems associated with these changes instead of an evident structural inju-ry.4 Signs such as cognitive impairment, memory deficits, shortened reaction times, or concentration difficulties can signal suspicion of concussion.9 Specifically, symp-toms can be categorized into 5 domains3,15,31:

� Cognitive – problems with memory and con-centration, inattentiveness, confusion, slowed reaction time.

� Somatic – dizziness, headache, nausea, photo-phobia, phonophobia.

� Mood – anxiety or nervousness, sadness, irritabil-ity, mood swings.

� Sleep – insomnia, sleeping too much, problems falling asleep.

� Physical signs – loss of consciousness.

Table 1

Sports Concussion Facts and Statistics23,24

Sport Incidence Notes

Field hockey High concussion rate for No. of participants, 1.4%

More concussions during competition than practice; 60% from equipment contact; 29% from player-to-player contact

Ice hockey High concussion rate for No. of participants, 3.9%

Higher concussion rate during competition than practice; 45% from player-to-player contact, others from ice, wall (glass)

Cheerleading . 27 000 ED visits in 2007; 20% of all injuries are concussions

Rising participation rates; higher risk of injury from more difficult tumbling moves; most head injuries occur during practice

Gymnastics 1.7% in high school gymnasts Concussions are 9 times more likely in competition than in practice; risk decreases slightly with age

Lacrosse 76% of male players from player-to-player contact; 9.8% of all female player injuries

Relatively low participation; higher concussion rate in competition than in practice for both sexes; rate decreased after helmets introduced

Volleyball 4.1% of all injuries during games 2 times more likely in games than in practices; most result from playing surface impact

Skiing/ snowboarding

9.6% of all ski injuries; 14.7% of snowboarding injuries

More recreational athletes than organized competition; similar head injury rates between both snow sports but more severe head injuries in snowboarders

Abbreviation: ED, emergency department.


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or learning disabilities.37 In addition, children and adolescents have different brain water content, degree of myelination, and anatomy that could affect biome-chanics of injury. As a result, children can take longer to recover from some concussion symptoms and potential long-term effects, especially from repeat concussions.38

Some evidence suggests that women have a different symptom pattern from concussions than do men. These reports have included greater incidence of fatigue, light-headedness, difficulty concentrating, and initial vision deficits compared with men. Men reportedly experience greater depression following concussions and more vomiting in the acute phase, although women tend to have the vomiting symptom in the subacute phase (about 8 days following concussion).9

Long-term SequelaeConcern is growing regarding the possible long-term

effects of sports concussions.22,39 A single concussion can lead to cognitive deficits in animal models 18 months following concussion.3 Chronic episodic memory deficits occur in a small subset of people with a history of concussion or more severe TBI.40

Another complicating factor in identifying postcon-cussion symptoms and helping assess injury accurately is that each individual’s perception of symptoms and subsequent reporting can vary. Psychological or social-psychological factors could lead to a person either magnifying symptoms or discounting them. A possible relationship might exist between mental health issues already present before concussion and problems with persistent anxiety following injury.33 Scientific evidence shows that concerns about long-term psychiatric com-plications in adults with concussion history are valid. Depression has been associated with retired athletes who had an average history of 3.97 concussions and who were an average age of about 59 years. There also is concern about chronic substance abuse and behav-ior changes in retired athletes, especially increased aggressiveness, but insufficient evidence exists on a rela-tionship to concussion history.6

Long-term effects and symptoms vary based on a second injury or a history of multiple concussions. Returning to physical or cognitive activity before full brain recovery can prolong symptoms and make a

resulting from impaired neurological function resolve spontaneously within the acute and subacute periods.4,15 Still, some athletes can experience symptoms such as depression or anxiety for months or years following a concussion.33

It is possible for a person with a concussion to have complications in the acute symptom phase. Seizure or an undetected injury in the brain parenchyma are examples. Brain parenchyma injury can cause hemor-rhage and hematoma, and an intracranial hematoma can further complicate seizure activity.4

Although confusion is a hallmark sign of con-cussion,19 fewer than 10% of athletes with sports concussions experience loss of consciousness.26 More often, concussions cause less evident symptoms in the 5 domains.15 If an individual has a known impact or inju-ry involving the head, any 1 or more symptoms in these domains suggests further assessment.31 Wasserman et al evaluated sports concussions in more than 1600 college athletes and found that headaches were the most com-mon complaint in concussions from nearly all organized sports studied, followed by dizziness and difficulty concentrating.34 The most common reported symptoms in the Marar et al study of high school athletes were headache, followed by dizziness, difficulty concentrat-ing, confusion, photosensitivity, and nausea.24 A high variability in concussion symptoms has led clinicians to abandon concussion symptom severity grading scales.21

Symptom recognition is critical to early assessment and diagnosis of concussion, yet athletes often dismiss their symptoms.35

Postconcussion syndrome is the name applied to 20% to 30% of patients with apparently mild closed-head (ie, the skull and dura matter remain intact)injuries but continued symptoms.9,36 It is marked by severe concussion symptoms that appear in the acute or subacute symptom phases (from a few weeks to months following injury) and persistent symptoms for up to 3 months.9,36 Students (elementary through college) with sports concussions often experience recurring or worsening symptoms after they return to play or to the classroom.7

Susceptibility to and recovery from concussions can be affected by pre-existing conditions such as genetic factors and a history of migraines, psychiatric disorders,


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aggressive behavior, poor impulse control, mood dis-orders ranging from apathy to anxiety, and suicidal thoughts or self-harm behaviors (see Figure 2).6

In 2016, researchers at the University of California, San Francisco noted a loss of brain volume associated with tau in midbrain regions asso-ciated with CTE. The researchers compared MR scans acquired 4 years apart on a 51-year-old man who had played football for 3 years in high school and in college summer camps for an estimated 900 blows to the head.42 Postmortem studies show tau-associated neurofibrillary tangles, along with glial tangles and neuropil threads.6

person more susceptible to lasting neurological dysfunction.2 Sports are particularly risky for long-term consequences of concussion from repeated head injury. It is esti-mated that professional football players receive between 900 and 1500 blows to the head each sea-son.32 Even repeated subconcussive blows lead to damage.41 Further, symptoms such as slowed reaction time or impaired cognitive ability could put an athlete at higher risk for concussions and neurologic injury, depending on the sport and circumstances of play. Players who have had multiple concussions can exhibit mild cognitive impairment, diffuse swelling, motor dysfunction, and mood disturbances years after concussive injuries.3,32

Chronic Traumatic Encephalopathy

In 2005, neuropathologist Bennet Omalu gave a name to the long-term neurological signs and symptoms caused by multiple concussive head injuries. Omalu performed autopsies on 3 former NFL players who had died at relatively young ages and found a pattern in their brains. Each former player had a high concentration of the protein tau. Tau is the protein also associated with Alzheimer disease. Omalu published his findings, calling the degenerative disease associated with tau and head injuries chronic traumatic encepha-lopathy (CTE).1

Observations of degenerative disease associated with a history of concussions have been made for many years, but Omalu defined the neuropathological process.1,3 By doing so, Omalu opened the door to additional research to explain late or long-term cognitive and psychiatric effects of multiple concussions.3,6 Among observed effects are memory and executive functioning problems,

Symptom overlap Pathological overlap

Concussion

Symptoms

PCS

CTE PSP CBSPD

FTDMNDLBD

ALS-PDC

PSPFTD

CBD

ALS-PDC

AD?

?

CTETau

Concussion CTE

AD

Beta-amyloid

LBD

Alpha-synuclein

PD

CTE

MND

TDPCTEFTD

PCS

Concussion

ALS-PDC

Figure 2. The interrelationships between concussion, postconcussion syndrome (PCS), chronic traumatic encephalopathy (CTE), and all the neurodegenerative diseases. A. There is considerable symptom overlap between concussion, PCS, CTE, and the neurodegenerative diseases. B. Pathologically, the relationship between concussion, PCS, CTE, and all the neurodegenerative diseases is unclear. In CTE there is substantial evidence for overlapping pathology of tau, TDP-43, amyloid, and alpha-synuclein with neurodegenerative diseases. In neurodegenerative diseases such as Alzheimer disease (AD), Parkinson disease (PD), and Lewy body disease (LBD), there is also overlapping pathology. The pathology of concussion and PCS and their relationship to CTE remains to be explored. Abbreviations: ALS-PDC, amyotrophic lateral sclerosis-parkinson dementia complex (Guam); CBD, corticobasal degeneration; CBS, corticobasal syndrome; FTD, frontotemporal dementia; MND, motor neuron disease; PSP, progressive supranuclear palsy. “?” indicates uncertainty about overlap. Reprinted with permission under the terms of the Creative Commons Attribution license. Tartaglia MC, Hazrati LN, Davis KD, et al. Chronic traumatic encephalopathy and other degenerative proteinopathies. Front Hum Neurosci. 2014;8:30.

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To date, the only definitive diagnosis for CTE is made after death, with postmortem tissue samples showing the disease’s unique pattern of tau deposition.45

Sideline AssessmentOn-field, or sideline, assessment is a method of deter-

mining whether an athlete should return to play after a potentially concussive impact or injury. Determining a high probability for concussion as soon as injury occurs is critical in sports concussions because of the effects related to a second concussion before the brain has recovered from the first.19,44 There often is tremendous pressure on athletes and those evaluating their injuries to return the player to competition. Athletes can be unaware of and show no signs of a concussion and can minimize or mask symptoms to hasten their return to play.4

A number of tools have been developed to improve this initial assessment. Most notably, the Sports Concussion Assessment Tool (SCAT) provides a side-line assessment approach to measuring acute symptoms or for evaluating injured athletes immediately after injury.44 The SCAT combines clinical assessment into a brief assessment of concussion during sports prac-tices or competition, and it has been through several revisions since its introduction in 2005.18 The most recent Zurich consensus statement recommends use of SCAT3 for evaluating adults and Child SCAT3 for evaluating pediatric athletes for concussion.31

Concussion assessment tools included in SCAT are: � Maddocks Sideline Questions–This series of

measures addresses the fact that many sports concussions do not cause loss of consciousness, which was a measure used in early assessment systems. Maddocks proposed using questions pertinent to the activity in which the athlete was participating instead of traditional questions to determine orientation (eg, What day is it? Who is the president?). Instead, sideline assessment can ask questions such as, “What quarter are we in?” or “Who did we play against last week?”20,31

� Graded Symptom Checklist–This assessment looks at subjective measures of preinjury and postinjury symptoms.44

� Standardized Assessment of Concussion–This tool was 1 of the first systems for sideline

The abnormal cortical tau deposition represents pathology similar to Alzheimer disease, but the associa-tion of tau and CTE to cognitive effects still is under study, particularly in relation to aging.6,43 Overlap exists between normal age-related cognitive decline and the pathophysiology of late effects of sports concussion, and it has been proposed that latent microstructural results of concussion in brain tissue make the brain more vul-nerable to aging-related decline.43

In the most recent Zurich consensus statement from the International Consensus Conference on Concussion in Sport, attendees concluded that CTE is a distinct tauopathy, and that incidence in athletes still is unknown. The statement also said that much needs to be ascertained about the cause-and-effect relationship of sports concussions to CTE.31

Strain et al showed an association between history of concussion with loss of consciousness in retired ath-letes who had reduced hippocampal volumes and poor verbal memory. The study’s retired athletes who had mild cognitive impairment tended to be older (about 63 years) and have a history of loss of consciousness with concussion.40 Studies also are being conducted to identify biomarkers associated with concussion in the acute phase and with CTE and diffuse white matter anomalies.41

Assessment and DiagnosisThe key to assessing concussions is initial observa-

tion of subjective and nonspecific symptoms.21,44 Some common symptoms of concussion are similar to those of other conditions, and variability among individual athletes’ symptoms is wide. In fact, the symptoms associated with concussion are so common that many people who do not have a concussion report that they are experiencing 1 or more concussion-associated symptoms during assessments. This includes 60% of male athletes and 48% of female athletes, according to 1 researcher.21 The lack of an objective measure compli-cates early assessment.20

In the past, sports concussion evaluation relied on observable symptoms and a neurological examination that included checking cognitive function and bal-ance.19 Although more thorough assessment tools are available for evaluating head injuries, the tools rely pri-marily on self-reporting and other subjective findings.20


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include similar medical history evaluation and prein-jury, or baseline, testing. Recommendations include a clinical examination and documentation of postural stability and neurocognitive measures. In addition, evaluating an athlete for common concussion symp-toms before play provides a baseline performance against which to compare postinjury evaluation.18

Athletes with head injuries also can be assessed in an emergency department or physician office.5,31 Nearly 80% of patients seen in the emergency department for head injury are treated and released, but about 20% have more severe injuries.35 Mild TBIs account for nearly 95% of head injuries.46 Therefore, although early assessment is critical to prevent further injury to the brain, many of the imaging examinations conducted to assess concussion are unnecessary.5,31,46

The Glasgow Coma Scale is used widely in emergen-cy departments to assign a score to head injuries. The assessment includes adding points for eyes that do not open, open in response to painful stimuli, or open to verbal commands. The assessment also measures abil-ity to speak clearly and whether the patient can move, such as extending limbs or moving away when exposed to painful stimuli. The assessment results in a numeri-cal score; a low score (3-8) indicates severe injury, and a higher score (13) indicates mTBI.47 Glasgow Coma Scale findings are then classified into mild, moderate, or severe categories based on the score.35

In emergency departments, use of imaging varies considerably, ranging up to nearly 42% for ordering head CT examinations to assess TBI. A 2014 study showed that trauma centers were more likely to order imaging examinations than were nontrauma centers.47 Utilization of CT to evaluate pediatric head trauma increased from 12.8% in 1995 to more than 28% in 2000, even though hospitalization rates for head trauma remained stable. Pediatric organizations, such as the Pediatric Emergency Care Applied Research Network, have developed clinical recommendations to assist physicians in identifying pediatric patients at risk for negative outcomes from TBI as well as low risk for mod-erate to severe TBI. The recommendations also help assist clinicians in diagnosis and imaging decisions. Signs and symptoms evaluated include level of altered consciousness, presence or absence of clinical signs of

assessment of sports concussions. The rapid assessment includes evaluating orientation, imme-diate memory, concentration, and delayed recall.18 This assessment has been shown to be sensitive at assessing sports concussions within the first 48 hours following injury.44

� Balance Error Scoring System–Maintaining bal-ance requires multiple sensory inputs and outputs to the muscles. Measuring postural stability is proposed as a method of sideline assessment of head injury. The assessment might not be as effective as others because balance recovers more quickly than other functions and because of wide variability in how observers rate balance.44

� Reaction time–Reaction time often is slower to improve following concussion and could prove helpful as a measure of neurological deficit. Computerized testing can be used clinically or on the sidelines; a clinical reaction time test can be performed without a computer.44

Sideline assessment can require evaluating an athlete in a locker room or other adequate facility. The assessment and final decision about potential concussion and clear-ance for activity should be based on clinical judgment and made by a physician or other licensed health care provider.31

Clinical DiagnosisBecause many concussion measures are subjective,

preparticipation or preseason examinations can provide baselines against which medical and sports personnel can compare postinjury assessment. A preparticipation examination should include questions about previ-ous concussions and evaluation of medical history, in particular, history of headaches, depression, or sleep problems. For example, knowing that an athlete has attention deficit hyperactivity disorder (ADHD) can inform later evaluation of symptoms. Although the reasons are unclear, injured athletes who have ADHD experience significantly higher rates of concussion diagnoses than do children who do not have ADHD. It is possible that typical neuropsychological measures of concussion (eg, speed of information processing, word f luency, and memory) can be affected by existing ADHD or learning disabilities. Preseason examinations


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reporting on findings, similar to the use of the Breast Imaging Reporting and Data System.49

In general, clinical diagnosis and grading of TBI involves31,47:

� Comprehensive injury and medical history. � Physical examination and comparison of clinical

status immediately after injury (ie, whether symp-toms have worsened).

� Neurological examination assessing mental sta-tus, cognitive function, gait, and balance.

� Neurocognitive (and sometimes neuropsycho-logical) testing.

� Determining whether imaging is needed to exclude severe TBI and structural abnormality.

Use of neuroimaging in evaluating mTBI might be more useful with advanced imaging methods and with a large database of images and findings on people who do not have TBI to which concussion and mTBI could be compared.13

Conventional ImagingConventional neuroimaging (CT and MR) is expect-

ed to be normal if used to evaluate patients who have a sports concussion.50 Pediatric neurologists, radiolo-gists, and sports concussion recommendations do not support the use of neuroimaging to diagnose an acute concussion without strong suspicion of intracranial injury.21,35,51 Morgan et al studied imaging results of 52 pediatric neurology clinic patients with postconcussion syndrome, 40 of whom had received a sports concus-sion. Only 5% of MR examinations and 13% of CT examinations yielded significant findings. Of 7 total findings on imaging, only 2 were related to the concus-sion.51

Despite the level of evidence studies and recom-mendations stating little value to imaging athletes with sports concussions using conventional structural imaging, a 2014 study showed lack of knowledge and consistency regarding imaging. White et al surveyed coaches and sports trainers involved in Australian football and rugby and found that a high proportion believed that postconcussion imaging could show concussion injury damage to the brain.10 The authors’ findings were consistent with a similar survey of Canadian hockey coaches.10

basilar skull fracture, headache severity, mechanism of injury severity, vomiting, and loss of consciousness.35

Role of Medical ImagingThe objectives of medical imaging following a head

injury are to help determine whether patients need emergency care or intensive surveillance, or to deter-mine prognosis in more severe head trauma.46 The metabolic chain of events from concussion is functional rather than structural, so neuroimaging typically is negative in patients following a sports concussion.36 Because of this and concerns about cost and risk vs benefit, the American College of Radiology and other societies have developed recommendations and guide-lines for use of neuroimaging in the diagnosis and management of concussion.47,48 Still, neuroimaging has a place in sports concussion evaluation, especially in research and clinical imaging of CTE and other chronic effects of concussion.13

ClinicalAccording to the American College of Radiology,

minor or mild acute head trauma (13 on the Glasgow Coma Scale) imaging usually is not appropriate as an initial study in diagnosing concussion.48 When imaging is indicated in head injury, the first examination chosen is CT without contrast. An MR examination without contrast might be indicated when a patient has new, persistent, or worsening symptoms.47 Pediatric neurolo-gists generally recommend use of CT and MR only for suspicion of moderate or severe TBI, intracranial hem-orrhage, evidence of skull fracture, or multiple or severe trauma.21

Conventional neuroimaging can falsely reassure physicians and patients by returning findings that do not indicate underlying functional problems.5 Since 2009, several entities have brought together experts in TBI to develop and refine a standard set of terminology and definitions to better characterize intracranial inju-ries.35 In early 2017, the Head Injury Institute worked on developing a Traumatic Brain Imaging Reporting and Data System to standardize reporting and data collection from imaging of TBI. The intent is to apply evidence-based protocols to provide appropriate imaging rationales across disciplines and standardize


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awareness of concussions and reported that despite increased visits and CT examinations, injury severity was low.52

Magnetic Resonance ImagingMR imaging is more sensitive than CT at detecting

small lesions in TBI.35 However, use of MR as a primary imaging modality for concussion is not recommended, partly because of availability and the inability to assess head injury patients rapidly under the constraints of MR accessibility.35 Most guidelines for concussion management reserve MR examinations for patients who have persistent and consistent symptoms or signs of focal neurological deficits.36 Still, the practice of acquir-ing MR scans for patients who have normal noncontrast CT results and persistent but unexplained neurological symptoms is common, despite a lack of evidence for clinical utility.35

Rose et al studied predictors for CT and MR use in a group of pediatric patients referred to a sport concus-sion clinic.50 Although use of CT generally followed standard clinical predictors for pediatric patients, acute signs and symptoms did not predict use of MR exami-nations. In most cases, ordering MR imaging in these patients was related to persistent postconcussion symp-toms.50

Typical pulse sequences for MR imaging of TBI include T1 weighting, T2 weighting, f luid attenuation inversion recovery, T2* gradient echo imaging, and diffusion-weighted imaging.35 MR with T2 weight-ing or T2W and f luid attenuation inversion recovery sequences have been shown to be more sensitive than CT without contrast in demonstrating epidural and subdural hematomas, small cortical contusions that are not hemorrhaging, brain stem injuries, and hemor-rhaging such as in axonal injury.21,35 Ellis et al reviewed records and CT and MR imaging reports of patients referred to a Canadian concussion program between September 2013 and July 2014. MR scans demonstrated hemorrhagic and nonhemorrhagic injuries that affected decisions about letting athletes return to play.36

MR spectroscopy, a form of multimodal MR imag-ing, has shown neurometabolic changes up to 1 month following sports concussion, even though the patients’ symptoms had resolved 2 weeks prior.20,53 The amino

Computed TomographyCT without contrast can serve as the initial triage

imaging examination for moderate to severe TBI but seldom is appropriate for mild TBI or a sports con-cussion.35,48 Shorter examination time requirements, tolerance of life support equipment during scanning, and ability to show signs of neurosurgical emergencies make CT the head trauma scan of choice.12 CT without contrast can demonstrate signs of severe injury such as intracranial hemorrhage, collection of f luid in the extra-axial space, skull fractures, cerebral edema, swelling, and herniation.35

Efforts to encourage judicious use of CT for con-cussion have intensified since 2001, particularly in evaluating children.15,35 Utilization of CT to evaluate minor head injuries increased in the late 1990s and early 2000s following release of studies reporting the rate of TBI in mild injuries to be as high as 13%, leading to more aggressive use of scanning.15 CT radiation dose to pediatric patients is of concern because children’s brains are more sensitive to ionizing radiation than adults’ brains and because head CT effects can increase the risk of cataracts later in life. Decisions regarding referral to CT for children who have a concussion gen-erally follow the Pediatric Emergency Care Applied Research Network rules. Several prediction rules also exist to help identify whether a possible intracranial injury requires CT evaluation and to help adults with low risk for detectable brain injury avoid noncontrast CT examinations.35

An analysis of the prediction rules evaluated CT use and results in children who were observed clinically for TBI before referring to CT and those sent directly to CT. Utilization was slightly lower in the observed group, but results of clinically significant injury were similar for both groups. Another study showed that delaying CT in favor of clinical observation in the emergency department (with the exception of signifi-cant injuries; these children received immediate CT examination) reduced the rate of CT utilization and subsequent dose with no delays in diagnosis.35 Zonfrillo et al reported that emergency department visits and use of head CT for concussion increased in a nationwide sample of emergency departments between 2006 and 2011. The authors attributed increased visits to public


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imaging with 3-D magnetization prepared gradient echo sequences followed by blood oxygenation level dependent (BOLD) images acquired with T2* weighted gradient echo-planar images. The authors found similar functional changes in brain activity of children who had concussion to adults who had concussion during working memory tasks. They found some differences, however, including reduced working memory accuracy compared with healthy controls.57

Neurovascular coupling suggests that increased neuronal activity leads to a rise in cerebral perfusion in the area. Increased blood f low alters the ratio of hemoglobin with and without oxygen and influences the BOLD signal.4 Properties of hemoglobin alter local magnetic susceptibility. Use of BOLD techniques pro-vides a means to noninvasively evaluate brain activity (see Figure 3).53

Cerebrovascular reactivity refers to the change in cere-bral blood flow in response to a stimulus. For example, decreases in cerebral blood flow of up to 50% have been demonstrated in patients with severe TBI, and it is theo-rized that insufficient delivery of blood coupled with other parts of the cascade of concussion effects account for the severe lack of neurometabolic energy following concus-sion. Neuroimaging studies have shown alterations in cerebrovascular reactivity in patients with moderate and severe TBI.58 In particular, functional MR methods have shown excellent potential in evaluating brain changes associated with behavioral and cognitive deficits.55 These studies support the possibility of examining cerebral blood flow with MR scans to evaluate concussion but lack sufficient evidence of routine clinical utility for functional MR imaging with BOLD in diagnosis and prognosis of concussion patients.55,58

Quantitative neuroimaging measures are more helpful than structural MR information in evaluat-ing concussion and recovery from concussion.56 Functional MR imaging techniques can localize neuronal activation in the brain’s gray matter during rest or a cognitive load, helping to evaluate functional brain networks.4,56

Diffusion Tensor ImagingDiffusion tensor imaging (DTI) is a well-established

technique in concussion evaluation, however, its

acid derivative N-acetylaspartate is a metabolite that exists almost exclusively in neuronal structures and can indicate their integrity. N-acetylaspartate diminishes in the brain following mTBI. Reductions in the metabolite are more severe following repeated concussions.20,54 MR spectroscopy has shown potential for aiding early prog-nosis for clinical outcomes of pediatric patients with TBI. Measures of reduced N-acetylaspartate have been correlated with long-term neuropsychological deficits in children.55

MR spectroscopy uses the same physical principles as MR, but data are converted and processed to cre-ate a spectrum of signal intensities. Images can be captured with single-voxel spectroscopy or chemical shift imaging. Although single-voxel technique has a higher signal-to-noise ratio, it requires accurate volume of interest placement because only a single spectrum is obtained. Chemical shift spectroscopy covers a larger area but takes longer to complete and has a lower signal-to-noise ratio.55 The technique has shown broad decreases in white matter and N-acetylaspartate of patients with mTBI and other findings but lacks suf-ficient evidence for MR spectroscopy sensitivity in routine clinical use for patients who have concussions.55

Functional Magnetic ResonanceResearchers continue to explore ways to use con-

ventional or widely available MR techniques in clinical assessment of TBI.35,56 Czerniak et al studied college athletes who had concussions within the previous 6 months along with a group of college athletes who had no history of concussion, using clinical interviews, neu-rocognitive assessments, T1-weighted MR techniques, and functional MR.56 The authors found that athletes who had a recent concussion performed similarly to those who had no concussion history on executive function tests, but on neuroimaging, their resting brain networks had significantly increased connectivity com-pared with the athletes who had not had a concussion in the previous 6 months.56

Keightley et al used functional MR examinations to evaluate working memory performance and related brain activity in youths who had concussions and a control group of healthy children.57 Participants had high-resolution T1-weighted, 3-D anatomical


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damage is measured using fractional anisotropy and mean diffusivity.47,55 DTI involves several metrics, and specialized data processing and analysis can translate the data to depict white and gray matter tract abnormalities.55 Fractional anisotropy measures diffusion along the longi-tudinal access of the axon, and mean diffusivity measures amplitude of overall diffusion regardless of direction. Methods of axial and radial diffusivity most likely illus-trate axonal and myelin loss (see Figure 4).43

Using DTI, Tremblay et al demonstrated the effect of concussion history in retired athletes. Their study revealed that aging brains of patients who have a history of concussion show a diffuse pattern of white matter anomalies.43 The data reflecting acute and chronic changes to the brain from TBI vary, however, and frac-tional anisotropy can indicate other disorders affecting white matter. Although more research is needed, group analyses have shown that DTI can detect alterations in the brain in mild to severe TBI.55

With diffusion spectroscopy, more accurate mapping of axonal trajectories can be produced. The technique requires comprehensive sampling, which can show het-erogeneity inside voxels and crossing of fiber tracts.55

usefulness in evaluating concussion is under investiga-tion.55 Recent reports have shown DTI as useful for detecting axonal injury that is too subtle to be seen with other imaging methods.19,47 DTI could provide the objective measures needed to better demonstrate focal ischemic lesions and diffuse axonal damage, although some controversy surrounds usefulness of the findings.19,59 DTI can provide information about the integrity of white matter tracts in the brain by measur-ing diffusion of water in voxels. Water tends to diffuse in the same direction as axonal fibers.4,19 With an intact neuronal axon, water particles move in a straight line from 1 end of the axon to the other, but when an axon is not intact, the particles move in various directions.4,47 The rate of voxel diffusion and preferred direction of diffusion can demonstrate injury to an axonal area.4,19,55 Axonal pathology is characteristic of long-term concus-sion history.3 The technique uses 6 diffusion gradient directions to compute the diffusion tensor.19

In chronic mTBI, a decrease in fractional anisotropy in the corticospinal tracts, sagittal stratum, and superior longitudinal fasciculus has been shown. These changes correlate with deficits in cognitive function.47 The axonal

Figure 3. Blood-oxygen level dependent images. Second-level analysis maps and postconcussion symptom scale scores for healthy control subject (A) and adoles-cent postconcussion syndrome patient (B). Second- level individual comparisons examined at the P 5 .005 level demon-strate no evidence of abnormal voxels in the healthy control subject compared with the atlas of normal controls. Quantitative patient-specific alterations in cerebrovas-cular responsiveness are demonstrated in the adolescent postconcussion syndrome patient. Reprinted with permission under the terms of the Creative Commons Attribution license. Ellis MJ, Ryner LN, Sobczyk O, et al. Neuroimaging assess-ment of cerebrovascular reactivity in con-cussion: current concepts, methodological considerations, and review of the litera-ture. Front Neurol. 2016;7:61.

A B


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accumulate in areas of neuroinf lammation or apopto-sis/caspase activity.47

Studies on use of single photon emission CT and PET for TBI typically evaluate cerebral blood f low

Future Advanced Neuroimaging MethodsConventional neuroimaging and neuropsychologi-

cal tests can fail to detect concussion injury, especially diffuse axonal injury.41 As research into advanced neu-roimaging techniques continues, it is possible that new ways to assess concussion and recovery will emerge.3 To date, however, little evidence exists to support the use of advanced imaging techniques in clinical diagnosis or prognosis for patients who have TBI.55 Some studies have demonstrated utility of advanced neuroimag-ing for showing microstructural and functional brain abnormalities in patients who have concussion, but little consistency exists across reported studies.21 Advanced neuroimaging can add to the body of research on the pathophysiology of sports concussion.3

Quantitatively demonstrating amyloid plaque deposition could help evaluate CTE on neuroimaging. This has been accomplished with use of a compound such as Pittsburgh compound B (PiB) or Florbetapir F 18, both of which assist in evaluation of Alzheimer disease plaques and can detect neurodegeneration.3 At the 2016 Traumatic Brain Injury Conference, Samuel Gandy reported on use of positron emission tomog-raphy (PET) in displaying characteristic CTE tau in the brain of a former NFL player who had a history of at least 22 concussions in his 11-year career. The former player’s MR scans displayed no scar tissue or atrophy.45 PET scans could prove effective at measur-ing use of medications to treat neurodegeneration from concussion.3 Other PET agents under study can

Figure 4. Ventricular enlargement in concussed partici-pants on diffusion tensor imaging correlate with increases in mean diffusivity and in periventricular axial diffusivity. Sagittal (A), coronal (B), and axial (C) slices of the regres-sion analysis between lateral ventricular volume (vCSF) and mean diffusivity (MD, blue) or axial diffusivity (pink) in concussed participants. D, E, F. Group interaction analysis on the relationship between ventricular volume and mean diffusivity. The results are thresholded at P , .05, corrected for multiple comparisons. Insets illustrate linear relation-ships at 1 example voxel. Reprinted with permission from Tremblay S, Henry LC, Bedetti C, et al. Diffuse white mat-ter tract abnormalities in clinically normal ageing retired athletes with a history of sports-related concussions. Brain. 2014;137(Pt11):3007.2016;7:61.

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D

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Figure 5. Example of a 3-D volume rendering single-photon emission computed tomography (SPECT) scan of the undersurface of the brain in normal control compared with a 12-year National Footbal League (NFL) player. While the control subject has symmetric activity, the NFL player has multiple defects in the inferior frontal and temporal lobes suggestive of concussion-related hypoperfusion. Reprinted under the Creative Commons Attribution Noncommercial license. Amen DG, Willeumier K, Omalu B, Newberg A, Raghavendra C, Raji CA. Perfusion neuroimaging abnormalities alone distinguish National Football League players from a healthy population. J Alzheimers Dis. 2016;53:239. doi:10.3233/JAD-160207.

Brain SPECT PerfusionHealthy Subject vs 12-Year NFL Player

Healthy SubjectFull, symmetrical activity

12-Year NFL PlayerLow frontal, temporal

lobe activity (arrows)


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� Quantitative volumetric imaging such as MR with 3-D isotropic short-echo time spoiled gradient echo sequences to evaluate atrophy associated with TBI.35,47

� Perfusion imaging, which uses PET, stable xenon-enhanced CT, single photon emission CT, or perfusion CT and MR techniques to show scat-tered perfusion deficits that can be correlated to neuropsychological and neurocognitive deficits or amnesia. Stable-xenon CT requires special, expensive equipment and is impractical for emer-gency settings. Perfusion CT is the most readily available perfusion method.

� Magnetoencephalography, which uses neuro-magnetometers around the head to collect data through hundreds of sensors in waveforms show-ing magnetic f luctuations. The technique has low spatial resolution but high temporal resolution.47,55

The use of advanced neuroimaging protocols in research is common, but protocols and database report-ing are not standardized. A 2014 workshop brought together physicians and researchers to reach consen-sus on how to proceed with recommendations on research standardization for several conventional and advanced neuroimaging sequences.13 Future clinical use of advanced imaging for concussion diagnosis and management depends on systematic review of these evidence-based studies.55

ManagementThe number of athletes, especially youth ath-

letes, seeking medical attention for concussions has increased since 2004 and likely will continue as awareness of sports concussion expands. Consensus statements regarding concussion management and safe return to play or other activities have been in development since 2005 and can assist primary care providers and subspecialists in managing concus-sions and minimizing long-term effects.61 These statements include the Concussion in Sport Group best practice recommendations, developed by an international panel of experts. However, Stoller et al reported in 2014 that implementation of consensus statement recommendations has been inconsistent across specialties.62

and metabolism.55 Amen et al demonstrated use of functional single photon emission CT perfusion imag-ing to show that specific brain regions among NFL players had abnormally low perfusion compared with control subjects (see Figure 5).60 Few studies have tried techniques beyond blood f low and metabolic map-ping, however. Once these modalities include mapping of specific ligands related to TBI, the next step could be evaluation of molecular biomarkers.55 The recent finding regarding PET’s potential role in evaluating CTE-associated amyloid tau could provide a definitive diagnosis in living patients who have a history of mul-tiple concussions and symptoms suggesting CTE.45

The use of biomarkers as indicators of sports concussion or CTE has been studied since 2000.41 Biomarkers can correlate to both brain function and structure.53 A literature review by Papa et al evaluated the use of biomarkers in imaging of TBI and concus-sions. Identified studies involved athletes aged 11 to 52 years who participated in 7 sports. The biomarkers included tau, glial fibrillary acidic protein, neuron-specific enolase, and others. The authors reported that several biomarkers have potential for determin-ing concussion severity or correlation to repeat injury, mechanism of injury, and postconcussive symptoms, but the markers have not as yet been validated by fur-ther study or cannot be compared easily because of variability in research methods. The authors concluded that once validated, biomarkers could help provide diagnostic and prognostic information and be com-bined with neuroimaging to assess how concussion effects evolve or how the brain recovers.41

Diffuse axonal injury imaging has been shown to detect microhemorrhages and demonstrate diffuse axonal injury. MR imaging with susceptibility weight-ing or gradient echo sequences can show microbleeds in the brain. The microbleeds appear as signal dropout on T2* gradient echo images, but resolution is better with susceptibility weighting. Measuring the number and volume of diffuse axonal lesions could help cor-relate with chronic depression and intellectual function problems.3

In addition to the techniques discussed above, pos-sible advanced neuroimaging methods for evaluating concussion and TBI include:


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the drugs can affect arousal and cognition negatively.21 Dizziness in the acute phase of concussion that persists might require evaluation and management based on whether the cause is benign paroxysmal position ver-tigo, migraine, or central vestibular system damage.5

Some studies have reported on use of catechol-aminergic and cholinergic agents to improve cognition following TBI, citing faster information processing with the drugs’ use. No significant evidence supports that use of the agents is superior to cognitive rest for patients with concussion. In fact, cognitive rehabilitation for patients who have more severe TBI usually involves practice and training on how to compensate for cogni-tive impairment.5 Research continues on the specific nature and duration of cognitive rest following concus-sion.62

Upon discharge from emergency or primary care, providers should give athletes, or their parents, clear instructions for second injury prevention, symptom monitoring, and follow-up care. Patients seen in an emergency department should follow up with their primary care provider.15

Return to PlayIt is important to educate those in physical con-

tact sports and sports involving collisions so that the athletes can understand how to prevent exacerbat-ing second or multiple injuries.20 The most recent International Conference on Concussion in Sport consensus statement (November 2012) recommends a gradual return to school and social activities before return to contact sports and no return to play the same day a concussion occurs (see Table 2). Studies have shown that some college and high school students who are allowed to play the same day as injury have delayed onset of neuropsychological deficits following concus-sion that might not be evident in a sideline assessment.31

In addition, studies are demonstrating longer recov-ery times than universally recognized, especially in youth and adolescent populations, where recovery times have been found to extend to up to 4 weeks in children and teens vs established theories of a typical 1 to 2 weeks.63,64 Although children should receive cogni-tive rest, pediatric neurologists do not support extended school absences.21

The first step taken when concussion is suspected is removing the athlete from risk of subsequent con-cussion until assessed on the sidelines and evaluated further if indicated. The next step is 24 to 48 hours of physical and cognitive rest, which is recommended by the main consensus statements for children and adults.20,21 During the first few days following concus-sion, cognitive activities, such as reading and computer work, can worsen symptoms or delay recovery, and student athletes should not attend school.62 The patient should begin activity gradually, based on symptom per-sistence or recovery.20 Although there is consensus on the physical and cognitive rest approach for concussion management, research on effectiveness of the strategy is sparse.31 Athletes’ mood and cognitive symptoms can worsen with prolonged rest, so monitoring of symptoms and low-level physical activity can improve recovery without increasing risk.20

Clinical and neuropsychological assessment of symptoms should guide evaluation and management. A treating physician should perform neuropsychological assessment that includes cognitive function, typically using computerized tools. Few athletes need formal testing from a neuropsychologist.31

No specific medications are recommended for con-cussion treatment, but medical therapy is relevant to treating symptoms.20,21 Over-the-counter pain relievers, such as nonsteroidal anti-inflammatory drugs, can help relieve headache in most patients with concussion. If headaches have migraine-like features, such as auras, physicians might prescribe triptans for acute relief, or prophylaxis for persistent migrainous headaches with the anticonvulsant topiramate, tricyclic antidepressants such as amitriptyline, beta blockers, or magnesium supplements until symptoms improve.20 Topiramate should be used carefully because of the drug’s effect on cognition, and continued use of analgesics and triptans can cause headaches. Opioids are not recommended for routine postconcussion headaches.21

Concussion patients who have sleep disturbances can benefit from education on removing distracting stimuli, avoiding caffeine, and other strategies. Those who have erratic sleep patterns might receive a light sleep aid such as melatonin, but prescription medica-tions such as sedatives are not recommended because


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Role of Imaging in ManagementCurrently, there is no established role for imaging

in monitoring symptoms and managing return to play or prognostic decision-making in sports concussions. Although DTI shows increasing promise as a manage-ment tool, results of studies have been inconsistent about use of DTI in concussions vs more severe TBIs. The distribution of diffuse axonal injury also varies significantly from 1 patient to another. One method for standardizing findings is to conduct preinjury or preseason DTIs on athletes and compare the baseline findings to examinations taken after injury.4

PreventionThe only modifiable risk factor for the neurocogni-

tive and behavioral symptoms related to concussion is further concussions; preventing a second injury is critical for athletes.2,15,21 Still, athletic trainers and team medical staffs are pressured to return athletes to sports participation prematurely. Kroshus et al surveyed athletic trainers and team physicians from 530 institutions that belong to the National College Athletic Association. More than half of the participants reported receiving pressure from coaches and athletes to return players to competition prematurely following concussion.66 An inherent conflict of interest exists for training and medical personnel who work for college or professional athletic departments, especially when

The decision to return an athlete to play following concussion should be individualized.2 Research and con-sensus statements do not define symptom resolution and clinical recovery adequately. Reliance on self-reporting from athletes is more subjective for determining concus-sion status than an established, objective clinical marker would be. Further, women and men have different recov-ery times, as do children vs adults.63 The return-to-play decision should be based on monitoring of symptoms and an athlete’s concussion history and should be guided by a medical professional but approached as a team (ie, coach-es, trainers, the athlete or parents, and physicians).65

Between 2009 and 2014, tools used by athletic trainers and other professionals to assess concussion and return to play readiness improved.34 Methods for determining status include balance assessment (Balance Error Scoring System) and Standardized Assessment of Concussion scoring. The Immediate Postconcussion Assessment and Cognitive Test evaluates 3 categories of signs of recovery or continuing symptoms. It includes a health history questionnaire, postconcussion symptom scale, and 6 tests that evaluate neurocognitive impair-ments (eg, memory, processing speed, attention, and reaction time).63 A more conservative approach for return to play usually is warranted when testing of balance or neuropsychological symptoms is not performed.31 In gen-eral, coaches and trainers never should risk an athlete’s safety by returning him or her to play too soon.23

Table 2

Athlete Return to Play Following Concussion2,15,31

Step Details Purpose

1. No activity Complete physical and cognitive rest, typically 24 to 48 h

Rest for recovery of injured brain

2. Light aerobic exercise

Light aerobic activity such as walking, swimming, stationary cycle; no resistance activity

Increase heart rate

3. Sport-specific exercise

Some typical drills for sport, but no contact activities such as practice games or tackles

Increase movement

4. Noncontact training drills

More involved drills and return to resistance exercises, but no contact

Allow exercise; monitor or improve coordination and cognitive load

5. Full practice Typical practice with contact, including scrimmage or practice games

Assess functional skills and restore confidence; reintegrate into contact at practice.

6. Return to play Normal game play, competition


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education.68 The Chuck Noll Foundation for Brain Injury Research was established in the name of a former NFL coach to fund research for understanding, pre-venting, and treating sports concussion.69 As of 2015, all 50 states have passed laws requiring that a medical professional clear youth for return to sports.21

ConclusionSeveral investigations are underway to evaluate

use of technology such as eye tracking, quantitative electroencephalography, and functional or advanced neuroimaging methods to diagnose concussion and assess recovery.31 Robotic prototypes made of foam are being tested to assist in football practices with less head impact.1 In neuroimaging, experts are developing protocols for using advanced neuroimaging for TBI and attempting to establish databases with evidence-based normative data for comparison.13 Future technologies such as advanced neuroimaging and biological markers could lead to improved evaluation and management of sports concussion.2

Teresa Odle, BA, ELS, is a health care writer and editor living in New Mexico. She has written numerous Directed Readings and health materials for consumers.

Reprint requests may be mailed to the American Society of Radiologic Technologists, Publications Department, 15000 Central Ave NE, Albuquerque, NM 87123-3909, or emailed to [email protected].

© 2017 American Society of Radiologic Technologists

References1. Schmidle N. Can technology make football safer? The New

Yorker website. http://www.newyorker.com/magazine /2017/01/09/can-technology-make-football-safer. Published January 9, 2017. Accessed January 9, 2017.

2. Harmon KG, Drezner JA, Gammons M, et al. American Medical Society for Sports Medicine position statement: concussion in sport. Br J Sports Med. 2013;47(1):15-26. doi:10.1136/bjsports-2012-091941.

3. Choe MC. The pathophysiology of concussion. Curr Pain Headache Rep. 2016;20(6):42. doi:10.1007/s11916-016 -0573-9.

4. Dimou S, Lagopoulos J. Toward objective markers of con-cussion in sport: a review of white matter and neurometa-

the staff reports to a coach or athletic manager instead of a physician. Addressing sports culture and sport-ing rules is a primary step in concussion prevention.2,23 Preparticipation examinations should be required before athletes participate in sports that add to risk of concussion.23

Although use of helmets in contact sports and sports such as cycling has prevented head lacerations, skull fractures, and intracranial bleeds, use of protective headgear has done more to minimize severity of TBI than to prevent concussions.2 No significant evidence suggests as of the 2012 Zurich conference that protec-tive equipment available for sports prevents concussion. It is possible that protective equipment use encourages false confidence and higher risk behavior, especially in young athletes. Still, there is consensus that protec-tive head gear or helmets should be worn for several sports to minimize TBI effects; this includes evidence supporting use of helmets for skiing, snowboarding, football, cycling, equestrian sports, and others.31

Prevention EffortsAlthough it is not possible to eliminate concussions

from most sports, steps can be taken to reduce the frequency and severity of the injuries.2 Rule changes and enforcement in sports likely prevent some concus-sions, although more study is needed on their effects.31 Limiting the amount of contact in practices can lower the number of concussions. In addition, studies have shown that athletes, parents, and coaches need more education to make informed decisions about con-cussion identification and prevention. Athletes in particular need to learn techniques that help minimize concussion and TBI from collisions or falls,2 although doing so can be difficult because of various biomechan-ics involved in concussion-related impacts.25

The intense focus on sports concussion and CTE has led to additional organized efforts to address the concerns. Best practice recommendations have been developed, along with student and coach fact sheets on concussions.67 Heads Up Football is a program piloted in 2012 that exists in more than 7000 youth and high school football programs as of 2017. The program includes coach certification, training of player safety coaches, and concussion recognition and response

https://doi.org/10.1136/bjsports-2012-091941

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17. McMains V. Signs of brain injuries in young NFL players adds to evidence linking concussions, CTE. Johns Hopkins University website. http://hub.jhu.edu/2016/11/29/brain -damage-repair-nfl-players/. Published November 29, 2016. Accessed February 26, 2017.

18. Resch JE, Kutcher JS. The acute management of sport concussion in pediatric athletes. J Child Neurol. 2015;30(12):1686-1694. doi:10.1177/0883073815574335.

19. Cubon VA, Putukian M, Boyer C, Dettwiler A. A dif-fusion tensor imaging study on the white matter skel-eton in individuals with sports-related concussion. J Neurotrauma. 2011;28(2):189-201. doi:10.1089 /neu.2010.1430.

20. Choe MC, Giza CC. Diagnosis and management of acute concussion. Semin Neurol. 2015;35(1):29-41. doi:10.1055/s-0035-1544243.

21. Rose SC, Weber KD, Collen JB, Heyer GL. The diagnosis and management of concussion in children and adolescents. Pediatr Neurol. 2015;53(2):108-118. doi:10.1016/j.pediatr neurol.2015.04.003.

22. Eckner JT, Kutcher JS, Broglio SP, Richardson JK. Effect of sport-related concussion on clinically measured simple reac-tion time. Br J Sports Med. 2014;48(2):112-118. doi:10.1136 /bjsports-2012-091579.

23. Daneshvar DH, Nowinski CJ, McKee AC, Cantu RC. The epidemiology of sport-related concussion. Clin Sports Med. 2011;30(1):1-17. doi:10.1016/j.csm.2010.08.006.

24. Marar M, McIlvain NM, Fields SK, Comstock RD. Epidemiology of concussions among United States high school athletes in 20 sports. Am J Sports Med. 2012;40(4):747-755. doi:10.1177/0363546511435626.

25. Clark MD, Asken BM, Marshall SW, Guskiewicz KM. Descriptive characteristics of concussions in National Football League games, 2010-2011 to 2013-2014 [published online ahead of print]. Am J Sports Med. 2017;45(4):929-936. doi:10.1177/0363546516677793.

26. Concussion care belongs at the top of every youth sports playbook. National Safety Council website. http://www.nsc .org/learn/safety-knowledge/Pages/Sports-Concussions.aspx. Accessed March 2, 2017.

27. Miller JH, Gill C, Kuhn EN, et al. Predictors of delayed recovery following pediatric sports-related concussion: a case-control study. J Neurosurg Pediatr. 2016;17(4):491-496. doi:10.3171/2015.8.PEDS14332.

28. USA Football commissioned research. USA Football web-site. https://usafootball.com/resources-tools/research -library/. Accessed March 3, 2017.

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5. Sharp DJ, Jenkins PO. Concussion is confusing us all. Pract Neurol. 2015;15(3):172-186. doi:10.1136/practneurol -2015-001087.

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7. Carson JD, Lawrence DW, Kraft SA, et al. Premature return to play and return to learn after a sport-related concussion. Can Fam Physician. 2014;60(6):e310, e312-315.

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10. White PE, Newton JD, Makdissi M, et al. Knowledge about sports-related concussion: is the message getting through to coaches and trainers? Br J Sports Med. 2014;48(2):119-124. doi:10.1136/bjsports-2013-092785.

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12. Shetty T, Raince A, Manning E, Tsiouris AJ. Imaging in chronic traumatic encephalopathy and trau-matic brain injury. Sports Health. 2016;8(1):26-36. doi:10.1177/1941738115588745.

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14. Bernhardt DT. Concussion: sport-specific biomechanics. Medscape website. http://emedicine.medscape.com /article/92095-overview#a7. Updated July 25, 2016. Accessed February 20, 2017.

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16. Guskiewicz KM, Bruce SL, Cantu RC, et al. National Athletic Trainers’ Association position statement:

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https://doi.org/10.1016/j.csm.2010.08.006

https://doi.org/10.1177/0363546511435626

https://doi.org/10.1177/0363546516677793

https://doi.org/10.3171/2015.8.PEDS14332

https://doi.org/10.1089/neu.2013.3050

https://doi.org/10.1089/neu.2013.3050

https://doi.org/10.1136/practneurol-2015-001087

https://doi.org/10.1136/practneurol-2015-001087

https://doi.org/10.1177/0706743716644953

https://doi.org/10.1212/01.wnl.0000438220.16190.42

https://doi.org/10.1080/00913847.2016.1142834

https://doi.org/10.1080/00913847.2016.1142834


https://doi.org/10.1177/1941738115588745

https://doi.org/10.3174/ajnr.A4254

https://doi.org/10.1097/MOP.0000000000000297


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42. Forrest W. MRI shows promise in diagnosing CTE in living patients. AuntMinnie website. http://www.auntmin nie.com/index.aspx?sec5prtf&sub5def&pag5dis&itemId5114942&printpage5true&fsec5sup&fsub5mri. Published August 23, 2016. Accessed August 24, 2016.

43. Tremblay S, Henry LC, Bedetti C, et al. Diffuse white matter tract abnormalities in clinically normal ageing retired athletes with a history of sports-related concus-sions. Brain. 2014;137(Pt 11):2997-3011. doi:10.1093 /brain/awu236.

44. Chin EY, Nelson LD, Barr WB, McCrory P, McCrea MA. Reliability and validity of the Sport Concussion Assessment Tool-3 (SCAT3) in high school and colle-giate athletes. Am J Sports Med. 2016;44(9):2276-2285. doi:10.1177/0363546516648141.

45. Underwood E. Can brain scans reveal concussion-linked disease? Science. 2016;352(6288):881. doi:10.1126/sci ence.352.6288.881.

46. Asadollahi S, Heidari K, Taghizadeh M, et al. Reducing head computed tomography after mild traumatic brain injury: screening value of clinical findings and S100B protein levels. Brain Inj. 2016;30(2):172-178. doi:10.3109/02699052.2015.1091504.

47. Wintermark M, Sanelli P, Le J. Ordering appropriate imag-ing for traumatic brain injury (TBI): everything you always wanted to know but didn’t have time to ask! Webinar presented at: American College of Radiology Head Injury Institute. October 21, 2015. http://www.headinjuryinsti tute.org/webinars. Accessed January 31, 2017.

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49. Standardization: TBI-R ADS. American College of Radiology Head Injury Institute website. http://www .headinjuryinstitute.org/tools/. Accessed March 1, 2017.

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29. American Academy of Pediatrics. Policy statement, tackling in youth football. http://pediatrics.aappublications.org /content/pediatrics/early/2015/10/20/peds.2015-3282.full .pdf. Published November 2015. Accessed March 8, 2017.

30. Safe Kids Worldwide. Game changers: stats, stories and what communities are doing to protect young athletes. https://www.safekids.org/sites/default/files/documents /ResearchReports/game_changers_-_stats_stories_and _what_communites_are_doing_to_protect_young_ath letes.pdf. Published August 2013. Accessed May 1, 2017.

31. McCrory P, Meeuwisse WH, Aubry M, et al. Consensus statement on concussion in sport: the 4th International Conference on Concussion in Sport held in Zurich, November 2012. Br J Sports Med. 2013;47(5):250-258. doi:10.1136/bjsports-2013-092313.

32. Concussion facts. Sports Concussion Institute website. http://www.concussiontreatment.com/concussionfacts .html#sfaq9. Accessed March 5, 2017.

33 Lange RT, Panenka WJ, Shewchuk JR, et al. Diffusion tensor imaging findings and postconcussion symptom reporting six weeks following mild traumatic brain injury. Arch Clin Neuropsychol. 2015;30(1):7-25. doi:10.1093/arclin/acu060.

34. Wasserman EB, Kerr ZY, Zuckerman SL. Epidemiology of sports-related concussions in National Collegiate Association Athletics from 2009-2010 to 2013-2014: symptom prevalence, symptom resolution time, and return-to-play time. Am J Sports Med. 2016;44(1):226-233. doi:10.1177/0363546515610537.

35. Wintermark M, Sanelli PC, Anzai Y, Tsiouris AJ, Whitlow CT; American College of Radiology (ACR) Head Injury Institute. Imaging evidence and recommendations for traumatic brain injury: conventional neuroimaging tech-niques. J Am Coll Radiol. 2015;12(2):e1-e14. doi:10.1016/j.jacr.2014.10.014.

36. Ellis MJ, Leiter J, Hall T, et al. Neuroimaging findings in pediatric sports-related concussion. J Neurosurg Pediatr. 2015;16(3):241-247. doi:10.3171/2015.1.PEDS14510.

37. Ketcham CJ, Hall E, Bixby WR, et al. A neuroscientific approach to the examination of concussions in student-athletes. J Vis Exp. 2014;8(94). doi:10.3791/52046.

38. Kinnaman KA, Mannix RC, Comstock RD, Meehan WP III. Management of pediatric patients with concussion by emergency medicine physicians. Pediatr Emerg Care. 2014;30(7):458-461. doi:10.1097/PEC.0000000 000000161.

39. Forrest W. Brain MRI shows lingering effects of concussion. AuntMinnie website. http://www.auntminnie.com /index.aspx?sec5prtf&sub5def&pag5dis&itemId5114718&printpage5true&fsec5sup&fsub5mri. Published July 22, 2016. Accessed January 3, 2017.

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https://doi.org/10.1227/NEU.0000000000001041

https://doi.org/10.1177/0009922815589915

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https://doi.org/10.1007/s00381-015-2916-y

https://doi.org/10.1089/neu.2013.2983

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https://doi.org/10.1007/s11682-014-9312-1

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4. Estimates show that as many as ______% of athletes report feeling no symptoms after a concussive blow to the head.a. 27b. 47c. 67d. 87

5. In 2005, a neuropathologist named the long-term effects of multiple concussive head injuries as:a. chronic traumatic encephalopathy.b. second impact syndrome.c. postconcussion syndrome.d. acute subconcussion syndrome.

6. Tools used to assess concussion rely primarily on:a. objective measurement of neurological function.b. the Glasgow Coma Scale.c. subjective and self-reported findings.d. neuroimaging.

1. Much of the public attention on sports concussion is focused on:a. acute effects.b. potential for severe traumatic brain injury (TBI).c. long-term sequelae and repeat concussions.d. faultiness of protective equipment.

2. Contrecoup head injuries result from ______ forces.a. low-energyb. shearc. direct-blowd. rotational

3. ______ is associated with more TBIs than any other sport.a. Soccerb. Skiingc. Boxingd. Football



continued on next page

10. MR with T2 weighting or T2W and fluid attenuation inversion recovery sequences have been shown to be more sensitive than CT without contrast in demonstrating:

1. epidural and subdural hematomas.2. small cortical contusions that are not

hemorrhaging.3. brain stem injuries.

a. 1 and 2b. 1 and 3c. 2 and 3d. 1, 2, and 3

11. Measures of reduced ______ have been correlated with long-term neuropsychological deficits in children.a. taub. N-acetylaspartatec. glial activityd. white matter

12. Fractional anisotropy measures:a. diffusion along the longitudinal access of the

axon.b. amplitude of diffusion with no regard to

direction.c. axonal loss.d. myelin loss.

13. ______ imaging has been shown to detect microhemorrhages in the brain.a. Magnetic spectroscopyb. Quantitative volumetricc. Diffuse axonal injuryd. Magnetoencephalography

7. Sideline assessment of sports concussion includes evaluation of:

1. orientation by using questions about game activity.

2. symptoms using a checklist.3. balance.


8. When imaging is indicated for head injury evaluation, the first examination chosen is:a. computed tomography (CT) with contrast.b. CT without contrast.c. magnetic resonance imaging.d. diffusion tensor imaging.

9. The greatest concerns regarding use of CT examinations in imaging concussions in pediatric patients are:

1. dose to the developing brain.2. increased risk of cataracts.3. missed structural pathology.




14. The first step taken when concussion is suspected is:a. 24 to 48 hours of rest.b. removing the athlete from risk of a subsequent

concussion.c. gradual return to activity.d. CT scan without contrast.

15. Concussion patients who have sleep disturbances benefit most from:

1. education about removing distracting stimuli.

2. prescription sedatives.3. light sleep aids such as melatonin.


16. Efforts to prevent concussions from most sports include:

1. limiting the amount of contact during practices.

2. providing concussion education to athletes, parents, and coaches.

3. changing and enforcing rules in sports. a. 1 and 2b. 1 and 3c. 2 and 3d. 1, 2, and 3

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neuroimaging of sports concussions...sports concussions teresa g odle, ba, els i n 2004, university...

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