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There is growing concern in sport medicine about the risks of chronic brain
dysfunction from repetitive concussions, yet the risk factors have not been
clearly identified. Recently, neuropsychological research methodology has been
utilized to systematically evaluate the cognitive effects of sport concussions.
This line of research has identified objective measures that are sensitive to
concussion and has shown that even a single mild concussion produces slowed
processing speed and memory difficulties during the first week post-injury.
Additionally, these studies raise concern about slow or incomplete recovery
following repetitive concussions. This article reviews the major studies of
acute and long-term effects of concussion in organized sports and the
application of neuropsychological evaluation to sport concussion. Introduction. Concussion is widely regarded as a
"transient post-traumatic
impairment of neural function."1 Anecdotal accounts by athletes about their
persisting post-concussion symptoms, and the development of dementia pugilistica
in former boxers, has raised concern about the risks of more permanent neural
impairment resulting from concussions sustained during sport.
Sport medicine personnel are confronted with difficult questions about the risks
of playing for athletes with concussion histories, however, risk factors for
chronic brain dysfunction from sport concussions have not been clearly
identified. Research efforts have been hampered by difficulties with objective
measurement of the subtle effects of concussions. Frequently, concussed athletes
perform normally on basic neurological examinations and have negative neuro-radiological
studies. Neuropsychological research methodology has been
recently introduced into sports medicine to systematically examine the effects
of concussions. Neuropsychology uses standardized tests to objectively measure
cognitive function. This line of research has been able to identify tests that
are both sensitive and specific to the effects of concussion and to recovery
from concussion. This article will review the major neuropsychological studies
of acute and chronic effects of concussion in organized sports and the
application of neuropsychological evaluation to the management of the concussed
athlete.
Acute Effects of Concussion in Sport. Neuropsychological studies of the acute
effects of sport concussion typically utilize
a pre-injury test/post-injury retest design.
At preseason, athletes complete cognitive tests that are sensitive to the
effects of concussion, i.e., attention, speed of processing and memory. They also
rate themselves on common concussion symptoms such as headache and dizziness.
This information provides a “baseline” for each athlete. When an athlete
sustains a concussion, he is retested and then compared against his baseline
scores. Serial retesting is frequently conducted at regular intervals to measure
recovery from the injury.
Football. The first large scale study of acute concussion in organized sport in
the US was conducted by Barth et al.2 Baseline evaluation, including symptom
inventory and neuropsychological testing of information processing speed, was
performed on 2300 college football players. Post-concussion evaluation was
conducted on 183 athletes. The concussed athletes exhibited increased symptoms,
particularly headache, and decreased performance on measures of processing speed
at 24 hours post injury. The cognitive deficits normalized between 5 to 10 days
post injury, but the post concussion symptoms showed a slower course of
improvement.
More recently, Collins et al3 conducted preseason symptom and neuropsychological
screening of 393 college football players. They found that learning disabilities
(LD)
or a history of 2 or more concussions independently contributed to lower
baseline testing scores. Athletes with both LD and prior concussions performed
even worse. Additionally, they found that 16 athletes
who sustained concussions during the season exhibited a verbal memory impairment
that persisted for at least five 5 days post-injury.
The National Football League (NFL) began conducting concussion research in 1996.
The research is a product of the NFL subcommittee on mild traumatic brain
injury. Team participation is voluntary and 22 teams are currently
participating. Baseline screening includes a concussion history, symptom
checklist, and neuropsychological screening.4 The protocol takes approximately
30 minutes to complete and focuses on testing of attention, processing speed,
and memory.
The baseline data is anonymously submitted to a database. Any athlete who
subsequently sustains a concussion is re-evaluated against their baseline data
within 24 to 48 hours
post injury. Serial re-evaluation occurs until the athlete’s symptoms and test
performance normalize. At present, approximately 1500 athletes have completed
baseline evaluation and post-concussion data is being prepared
for analysis.
Overall, research on collegiate football players suggests that single mild
concussions produce acute impairments of processing speed and memory that
rapidly improve during the first 5 to 10 days post injury. Athletes with
learning disabilities and multiple concussions may be at risk for slower or less
complete cognitive recovery. There is no research to date that has analyzed the
effects of repeated concussions in a large sample of football players.
Rugby and Australian Rules Football. Maddocks5 evaluated 75 Australian rules
football players during the preseason using a speed of processing test and
followed 13 players who sustained concussions during the season. He found
visuomotor slowing deficits immediately post injury that significantly improved
during the week post injury. Several players who were more moderately concussed
demonstrated a prolonged recovery period. Hinton-Bayre et al6 conducted
preseason baseline testing of processing speed on 54 rugby league players and
followed
10 players who sustained concussions during the season. This study also found
visuomotor speed impairment that persisted for up to
10 days. Additionally, this study found speed of processing deficits on more
complex
verbal tasks that persisted for up to 3 weeks post-injury.
Research on concussed rugby players has yielded results similar to American
football players. For a single mild concussion, visual processing speed deficits
are evident immediately after injury and significantly improve during the first
week post injury. Rugby research also suggests that complex processing speed
recovers slower and that more moderately injured players recover slower.
Hockey. No formal neuropsychological studies of the effects of concussion in
hockey players have been published. Since 1997, however, the National Hockey
League (NHL) has conducted a league wide concussion research project. The
project consists of preseason baseline screening for every athlete, including
concussion history, concussion symptom checklist, and neuropsychological testing
of attention, speed of processing, and memory.7 Players sustaining concussions
are re-evaluated within 24 to 48 hours after a concussion and are serially
re-evaluated every
5 to 7 days until symptoms and test scores normalize. Approximately 1500 NHL
players have completed baseline testing. The post concussion data is being
prepared for analysis.
Chronic Effects of Concussion in Sport. The effects of repetitive subconcussive
and concussive blows to the head on the development of chronic brain dysfunction
have been examined for several sports. Two primary research methodologies have
been used: 1) a matched control design that compares high and low risk athletes’
performance on specific symptom inventories and cognitive tests to low risk
athletes and 2) a single group design that analyzes relationships between the
athlete’s performance on cognitive tests and potential mediating factors, such
as length of exposure to the sport and injury history.
Boxing. Boxing is unique as a sport, since the primary goal is to deliver a
concussive blow to an opponent, ie, knock him out. Athletes participating in
boxing sustain repetitive subconcussive blows during the course of their career,
and many sustain concussive blows. The risk of chronic brain dysfunction
(dementia pugilistica) from boxing has long been recognized, but the sport
remains popular. At the amateur level, research that has compared boxers with
matched controls has produced mixed results. McLatchie et al8 compared 20
amateur boxers to an equal number of orthopedic control patients and found
impairments on measures of attention, reaction time, and memory. Kemp et al9
compared 41 amateur boxers to
27 non-boxing controls and found impairments on reaction time and pattern
recognition. In contrast, other studies have failed to detect significant
differences between boxers and controls on measures of cognitive abilities.10
Stewart et al11 evaluated 484 boxers at baseline and prospectively re-evaluated
393 of them 2 years later. At baseline, they found significant correlations
between the total number of bouts fought prior to baseline and the boxers
performance on memory and visual perceptual testing. They did not find any
significant relationships between boxing exposure and cognitive changes during
the 2 year follow-up period, and hypothesized that there may be a longer latency
period before cognitive deficits become manifest.
At the professional level, Ryan12 estimated that 9% to 25% of boxers eventually
become “punch drunk.” Multiple risk factors have been identified for the
development of dementia pugilistica, including retirement at a later age, longer
careers, greater number of bouts, poor performance, being a “slugger,” being
able to “take a punch,” and history of KO and TKO.13 Studies on the
neuropsychological effects of professional boxing have been fraught with
methodological problems that limit their conclusions. It is very difficult to
adequately control for the myriad factors that could contribute to cognitive
decline in boxers. One recent study that attempted to control for many of the
methodological problems was conducted by Jordan et al.14 They tested 42
professional boxers and found strong correlations between the amount of time
sparring and impairments on measures of attention and memory. They concluded
that exposure to repetitive subconcussive blows, as measured by amount of time
sparring, was more strongly associated with cognitive deficits than was age,
boxing record (win/loss), length of career, or history
of knockout/technical knockout. Overall, the research on boxers suggests a
strong relationship between boxing exposure and a decline of cognitive
abilities, particularly attention, speed of processing and memory.15 This
decline is not only related to concussive injuries, but also to repetitive
subconcussive blows.
Soccer. As in any contact sport, soccer players are susceptible to concussions.
They also sustain repetitive subconcussive blows by heading the ball. Concern
has been raised about the potentially detrimental effect of heading the ball as
well as concussion in soccer. Several studies have been conducted at both the
amateur and professional level with mixed results. One study of amateur athletes
compared 33 soccer players with 27 matched noncontact athletes and found
impaired performance on measures of planning and memory that were correlated to
the number
of concussions.16 At the professional level, Matser et al17 compared 53
professional soccer players with 27 elite noncontact athletes and found
impairments on measures of planning and memory that correlated to the number of
concussions and to the frequency of heading. Jordan et al18 compared 25 members
of the United States National Soccer Team and 20 age-matched control athletes on
MRI and a head injury questionnaire. On MRI, 9 of the soccer players and 6 of
the track athletes had positive findings. On the head injury symptom
questionnaire, the soccer players with prior concussions reported significantly
more symptoms, but there was no correlation between heading and symptoms. They
concluded that if there was a risk of chronic dysfunction in soccer players,
concussion, rather than heading, was the main factor.
Overall, preliminary evidence suggests that participation in soccer may result
in neurocognitive changes, but these studies have methodological problems that
limit conclusions. Longitudinal, large-scale research is necessary to answer
questions of soccer-related cognitive deficits resulting from heading versus
concussive injuries.
Clinical Neuropsychological Evaluation of the Athlete. At present, there are no
clear guidelines to indicate when an athlete should be referred for
neuropsychological screening as part of a concussion work up. Since research has
shown that these tests are sensitive and specific to the effects of sport
concussion, neuropsychological evaluation may be useful whenever objective
information is needed about the athletes’ neurocognitive status for clinical
decision making. Kelly19 recommends neuropsychological evaluation when the
athlete has sustained a concussion with loss
of consciousness, has confusion that lasts longer than a few minutes, has
amnesia that persists beyond the end of the game, has sustained multiple
concussions, or has an
overt change in behavior.
Traditional neuropsychological assessment typically involves several hours of
comprehensive testing across the domains of intelligence, academic performance,
attention, learning, memory, abstract reasoning and problem solving, language,
visuospatial functions, and sensory and motor skills. These lengthy batteries
are clearly not feasible for large-scale athletic programs. Brief sport
concussion neuropsychological screening protocols have been developed. The
sports concussion screening protocols typically acquire data about concussion
history (Table1), orientation, neurobehavioral symptom severity (eg, headache),
attention, processing speed, and memory (Table 2). For a single, uncomplicated concussion, a brief neuropsychological screening, conducted within 24 to
48 hours post injury, will be able to provide basic information about the
athlete’s symptoms and cognitive functioning. The evaluation, which is
conducted by a neuropsychologist, typically requires approximately 30 minutes of
testing. The test results are compared to norms appropriate to the athlete’s
age. This type of evaluation will provide information about the player’s
performance on cognitive tests in comparison to normative peers. If any
cognitive deficits are identified, then follow-up testing within 5 to 7 days is
useful to monitor recovery and to track any persisting problems. This systematic
evaluation of the concussed athlete will help to identify those requiring more
extensive neuropsychological and medical evaluation. Symptoms and scores should
normalize before the athlete returns to play. Athletes who have sustained
multiple concussions, or who have sustained concussions with persisting
symptoms, will require more extensive evaluation as part of the medical work-up.
Table 1. Concussion Symptoms Scale
Rating:
|
None
|
Mild
|
Moderate
|
Severe
|
|
|
0
|
1
|
2
|
3
|
4
|
5
|
6
|
CONCUSSION SYMPTOMS |
Base
|
Date
|
Date
|
Date
|
Date
|
Nausea
|
|
|
|
|
|
Vomiting
|
|
|
|
|
|
Headache
|
|
|
|
|
|
Dizziness
|
|
|
|
|
|
Blurred or Double Vision
|
|
|
|
|
|
Balance Problem
|
|
|
|
|
|
Trouble Falling Asleep
|
|
|
|
|
|
Sleeping More Than Usual
|
|
|
|
|
|
Drowsiness
|
|
|
|
|
|
Low Energy
|
|
|
|
|
|
Sensitivity to Light
|
|
|
|
|
|
Sensitivity to Noise
|
|
|
|
|
|
More Emotional Than Usual
|
|
|
|
|
|
Irritability
|
|
|
|
|
|
Sadness
|
|
|
|
|
|
Nervous/Anxious
|
|
|
|
|
|
Numbness or Tingling
|
|
|
|
|
|
Feeling Slowed Down
|
|
|
|
|
|
Feeling Like "In a Fog"
|
|
|
|
|
|
Difficulty Concentrating
|
|
|
|
|
|
Feeling "Pressure in Head"
|
|
|
|
|
|
Difficulty Remembering
|
|
|
|
|
|
Other
|
|
|
|
|
|
Total
|
|
|
|
|
|
Table 2. Acute Neuropsychological Evaluation Protocols.
|
Scale |
Description |
|
Orientation Scale (a,b) |
General Orientation |
|
Symptoms Checklist (a,b) |
Symptoms |
|
Hopkin’s Verbal Learning Test – Revised (a,b) |
Verbal Memory |
|
Brief Visuo-Spatial Memory Test – Revised (a,b) |
Visual memory |
|
Symbol Digit Modalities Test (b,c) |
Visual Processing Speed |
|
Trails A & B (a) |
Visual Attention |
|
Color Trails 1 & 2 (b) |
Visual Attention |
|
Controlled Oral Word Association Test (a, b) |
Naming |
|
Wechsler Adult Intelligence Scale B III
|
Digit Span (a,c) |
Attention Span |
|
Digit Symbol (a) |
Verbal Processing Speed |
|
Symbol Search (a) |
Verbal Processing Speed |
|
Pennsylvania State University Symbol Cancellation Test (b) |
Visual Scanning |
|
Speed and Capacity of Language Processing Test (c) |
Verbal Processing Speed |
|
|
a=NFL b=NHL c= Australian Rugby |
While comparing the athlete’s performance on cognitive tests to normative
peers is a standard neuropsychological practice and provides useful information
about the athlete’s cognitive status, comparing the athlete against his own preconcussion baseline provides the most sensitive
method for detecting subtle cognitive changes from concussion. Establishing a
preseason baseline is important because athletes vary considerably in their
cognitive abilities, making it difficult to discern if any subtle deficits that
are identified on post-concussion testing are attributable to the concussion or
to other unrelated factors. Preseason baseline screening enables the athlete to
act as his own control. Baseline screening is recommended whenever possible and
is being used at the high school, college, and professional level.
Conclusion. Neuropsychological studies of acute concussion have demonstrated
increased symptoms, slow processing speed, and memory impairments that persist
for at least 5 to 10 days and up to 3 weeks post-injury. Additionally, studies
of the chronic effects of concussion suggest that repetitive subconcussive and
concussive injuries may both independently contribute to persisting symptoms and
cognitive decline. These are important considerations for the clinical
management of the concussed athlete. Neuropsychological evaluation of athletes
provides a systematic approach for monitoring symptoms and cognitive changes
associated with concussion in both research and clinical applications. At the
research level, large scale longitudinal studies will be important for answering
questions about classifying injury severity, determining the effects of
repetitive injuries, and identifying risk factors for slow or incomplete
recovery from concussive injuries. At the clinical level, brief
neuropsychological evaluation provides a sensitive method for measuring the
acute and cumulative effects of concussions and is being used with increasing
frequency by sports medicine personnel in the management of concussed athletes.
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