Sports neurology

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Sports neurology

Paul McCrory, Erik Matser, Robert Cantu, and Massimo Ferrigno

Football neurology
Paul McCrory, Neurologist, Centre for Health,
Exercise & Sports Medicine and the Brain Research
Institute, University of Melbourne, Australia
For 15 years, I worked as a doctor for a team that played in
the Australian national “Aussie rules” football competition.
Since then, although not constrained by a single team
commitment, I have continued to look after individuals at
an international level in rugby league, rugby union, and
soccer.
My first, and in many ways most memorable, moment
came in my very first match as a team doctor. At that time, I
was an inexperienced medical graduate who had just
completed his internship. A colleague had asked me to fill in
while the regular team doctor (a dermatologist, no less) went
Figure 1. Collapsing scrums can cause spinal-cord injuries.
to England to further his postgraduate training. To my
horror, a player went down in a collision close to where I was
sitting. Without knowing any better, I ran straight onto the benign, such concussive convulsions or impact seizures
field. My first lesson was in personal safety when, by remain the most dramatic accompaniment of the concussive
narrowly missing being a casualty myself, I realised that state.2 Although unreported in medical journals, sports
professional footballers are considerably bigger and faster trainers—who are usually the first to the scene of any on-field
than I could ever hope to be. Perhaps that is why the injuries—saw the convulsive manifestation as commonplace.
mnemonic “DRABC” has ‘danger’ as the first item on the list It is just that doctors were too slow to get to the injured
of first aid priorities. Having arrived breathless and athlete to ever witness them! Thank goodness for TV
undamaged at the side of the unfortunate athlete, I saw that videotape. Researching football-related concussive
he was laying still and not breathing. My initial thought was convulsions also made me unique amongst my PhD peer
that he was dead. Years of medical training had left me group, who were following the more traditional neurology
totally unprepared for real-life medical emergencies outside research streams. The idea that watching sports videotapes
a well-equipped emergency department. Lesson number could be construed as research caused much envy at the time.
two: first aid skills are of far more use in sports medicine Just to show that sports neurology can throw up
than being able to do a neurological exam. To my complete surprises—soon after my initial experience, I ran out to a
surprise, the player soon woke up and we somehow downed player to find him feigning unconsciousness after a
managed to get him off the field so that the game could collision. This catatonic state related more to a
continue. disagreement with the coach than to any primary cerebral
Having very quickly realised that I had little knowledge pathology. Not surprisingly, his elite football career was
of this common injury, I attempted to rectify this deficiency. fleeting.
Unfortunately, none of the existing sports medicine On-field sports medicine can also be a hard taskmaster.
textbooks helped me. To my chagrin, most neurology books Professional sport presents many different ethical and
do not even list concussion as a disorder. Discussions with management challenges that simply do not occur in any
more experienced sports-medicine colleagues made me other mode of medical practice. Coaches, especially in
realise how little was known, and that any management professional teams, apply extreme pressure for rapid and
recommendations were purely anecdotal. This last point led hopefully accurate decision-making. In a situation of
me to over 20 years of research on sports-related concussion. deciding between a player with obviously broken ribs or a
In 2004, we can safely say that we now at least have an recovering concussion remaining on the field while another
international consensus on the definition and management player is stitched (or stapled) up on the sidelines, many
of this common injury.1 factors must be weighed in an instant.
Along my journey as a neurologically trained team doctor, Football also gets neurologists involved in the realm of
I witnessed some convulsions during concussion. Although spinal injuries. Debate continues to rage on both sides of the

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 Forum Sports neurology

Atlantic about the contribution of congenital cervical canal

stenosis to spinal-cord injury in sport. Of far more concern
is how organisations justify changes in safety on medical
grounds. 20 years ago, the sport of rugby union believed that
spinal-cord injuries were becoming more frequent and that
collapsing scrums (figure 1) were the cause of most injuries.
As a result, changes to scrum engagement rules were
introduced to de-power the force of the scrum. Did it work?
We have no way of knowing because there is no
epidemiological data of injury rates before and after this
intervention.3 This should be a salutary lesson for all
budding sports-injury epidemiologists.
Peripheral-nerve injuries are also common to all types of
rugby. With frequent body contact, both legal and illegal, the
peripheral nervous system often bears the brunt of this
trauma. Virtually every type of nerve entrapment or nerve
injury has been described in sport. The distinguishing
feature of sports neurology is not the diagnosis as much as Figure 2. Chronic brain injury in boxing—boxing dementia—can be
detected by neuropsychological tests.
the management. Elite athletes have competition deadlines
that often necessitate rapid investigation and aggressive
management strategies. For example, a rugby player who neurological health issues in boxers (figure 2)—acute brain
was on the verge of national selection suffered an axillary- injury, the insidious process of boxing dementia, the
nerve injury associated with a shoulder dislocation. Rather detection of chronic brain injury in boxers at a very early
than waiting the usual several months to assess recovery stage, prevention of cumulative chronic brain injury, and,
electrophysiologically, we opted to do an early surgical last but not least, motivation for boxers.
neurolysis with intraoperative nerve recording. This
confirmed that the axillary nerve was both intact and Acute brain injury in boxing
functional. Obtaining this information meant that his Given that the infliction of acute brain injury is one of the
rehabilitation could proceed aggressively. He rewarded our intrinsic aims of boxing, little or no research has been
faith by competing soon after in spite of recovering, but done on the symptomatology and prevention of such acute
incomplete, function of his deltoid muscle at the time of his injuries. Brain injury in boxing is very difficult to identify
selection. in the acute phase because of differences in concussion
Boxing and, to a lesser extent, soccer, are of particular guidelines and the absence of abnormalities on MRI.
neurological interest. Repetitive head impact is a feature of The Netherlands currently uses the symptom
both sports, yet only boxers seem to show evidence of classification system set out in the Guidelines on the
chronic brain injury. To be fair, the data about chronic brain Diagnosis and Treatment of People with Slight Cranial
injury in boxing is surprisingly slim and largely relates to Brain Injury.6 However, this scoring system is intended for
boxing as it was practised 70 years ago. We have also come to use by physicians. In addition, for international and
realise that genetic factors play an important part in the Olympic boxers, there are different grading systems for the
genesis of such states.4 In soccer, although it is often severity of brain injury in several countries,7 which has
anecdotally noted that similar disorders may develop, the confused international and Olympic communication about
evidence for such chronic problems is not compelling.5 neurological issues concerning traumatic brain injury. As
Although my sports medicine career was accidental, my an example, the guidelines for concussion published by the
formal training in neurology has led to a different approach American Academy of Neurology (AAN)8 in 1997 are
to many common sporting problems compared with my different to the guidelines presented by the Netherlands
sports-medicine trained peers. It has also led me into an Association for Neurology.6 In my opinion, the system
unexpected academic career at the borderlands between developed by the AAN should be adopted in international
these two areas. sports medicine because this system is very suitable for use
in the detection of brain injuries sustained in boxing and
Dealing with neurological injuries in sports: other contact and collision sports with a high risk of brain
boxing under debate injury. The AAN guidelines not only deal with loss of
Erik Matser, Neuropsychologist, St Anna Hospital, consciousness, like most of the European guidelines, but
Geldrop and Erasmus Medical Center, also focus on mental changes such as post-traumatic
Neurosciences Department, Netherlands amnesia without loss of consciousness after impact.
Since 1990, when the Dutch Government set up strict rules Most of the acute brain injuries in boxing are
for health issues in contact sports, I have been involved in dominated by neuropsychological changes. As an example,
mandatory annual neuropsychological testing of all I tested a large number of amateur boxers in Holland and
professional and top-ranked amateur boxers in the New York State before and after a boxing bout. On
Netherlands. I would like to discuss several difficult average, one in eight amateur boxers were concussed

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 Sports neurology
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during their bouts, and all CT scanning or MRI scans Prevention of chronic brain injury in boxers
showed no abnormalities. No EEG changes in concussed Neuropsychological testing is needed to detect chronic brain
boxers were detected, even some days after the bout. injury in boxers as early as possible. A boxer with chronic
However, the prefight and postfight neuropsychological brain injury, as indicated by slight cognitive dysfunction, can
test results showed substantial changes in attention, thus be advised to refrain from boxing activities that might
planning, and memory scores. It seems that most of the aggravate the neurological injury. Neuropsychological
acute brain injuries sustained in boxing are testing is always best done against an individual’s own
neuropsychological in nature. In addition, simple tests of baseline data, rather than against group averages. This is of
equilibrium were also sensitive in detecting symptoms of major importance especially with boxers, as most of them
acute brain injury in concussed boxers. In my opinion, are from different cultural and socioeconomic backgrounds.
MRI cannot be regarded as the gold standard in the It is important that boxers should have neuropsychological
detection of acute brain injury in athletes. tests as early in their sporting career as possible for the
purpose of gathering baseline data.
Chronic brain injury in boxing The annual examination of boxers should include
From annual follow-up, there is a clear linear association neuropsychological assessment. When symptoms of brain
between length of boxing career or the total number of injury appear, the boxer should stop at the right time. When a
sparring sessions, and the course and severity of chronic boxer shows signs of acute brain injury, the bout should be
brain injury. stopped immediately and the boxer should rest until he is
In an analysis of the insidious process of chronic brain recovered to his own baseline. When showing slight cognitive
injury in boxers, the number of sparring sessions was more impairments resembling mild chronic brain injury, the boxer
sensitive in predicting the severity of chronic brain injury should refrain from boxing.
than either the number of bouts or, surprisingly, the Motivation and education should be discussed with
number of knockouts incurred during fights. Repeated boxers. Most boxers are highly motivated to box, and they
subconcussive blows, in a short time, were more damaging all have a deep desire to go to the top. Most of them do not
to the brain than a single concussive blow. have any knowledge of brain injury—for example,
In tests of a large number of boxers, neuropsychological knockouts (concussions) are not considered dangerous but
and behavioural changes were most prominent in the early just part of the sport. Few coaches, boxing trainers, and
stage of chronic brain injury. Most of the boxers showed boxers realise that knockouts, mental changes, and amnesia
accumulation of frontotemporal neurocognitive changes are all symptoms of brain injury. In addition, there is little
(planning, attention, and memory problems) in realisation that the number of matches and sparring
combination with frontal behavioural changes (impulsivity sessions is positively associated with the severity of brain
and aggression). In my database, 90% of all Dutch injury. Education of coaches, boxing trainers, and boxers
professional boxers tested had these problems. In addition, should be a priority. All people participating in boxing
in the early stages of chronic brain injury, most of the MRI should be fully informed about the associated health risks,
and CT scans showed no abnormalities. When professional in particular the risk of chronic brain injury. Participation
boxers are not stopped in the early stage of chronic brain in contests should only be allowed when the risks are known
injury, 45% will develop severe chronic brain injury, which and accepted.
can be detected on MRI or CT. Moreover, one in five
professional boxers showed mild or severe problems in Should professional boxing be banned?
activities of daily living after the age of 30 years. Many If it is not possible to implement the measures outlined
professional boxers, who do not stop at the right time, will above, or if it is concluded that the recommended rule and
develop these symptoms of “punch drunk syndrome” procedure changes are unlikely to have any significant effect
(boxing dementia). “Punch drunk” boxers show a on the occurrence of brain injury, I would recommend the
combination of severe neurocognitive and behavioural prohibition of professional boxing. Professional boxers do
problems in combination with motor problems more sparring, they box matches with more and longer
(parkinsonism) and psychiatric symptomatology, mostly rounds, they don’t wear headgear, have less medical
paranoia. In most patients, the insidious process of severe supervision, and last but not least, are given financial
chronic brain injury in boxers starts with mild cognitive incentives, which makes them more vulnerable to severe
impairment, which develops into severe neurocognitive brain injury than amateur boxers.
deterioration and behavioural and psychiatric changes.
Moreover, there seems to be an association between Concussion severity should not be determined
neurocognitive deterioration and MRI changes. Most boxers until all postconcussion symptoms have abated
who present abnormal scanning results in my database have Robert Cantu, Neurosurgeon, Emerson Hospital,
scores more than two standard deviations under their own Concord, MA, USA
precareer scores in planning, attention, and memory. In Concussion is the most common sport-related head injury.
boxing dementia, it seems that neurocognitive and Today, sport-related concussion is a widely recognised
behavioural functions deteriorate first, and that major public-health concern in the USA and worldwide.
morphological changes in the brain, in combination with Initially, it was thought that concussion produced only a
abnormal motor and psychiatric symptoms, develop later. temporary disturbance of brain function caused by

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 Forum Sports neurology

Post-concussion signs and symptoms Cantu evidence-based grading system for concussion17
Depression Grade 1 (mild) No LOC PTA <30 min, PCSS <24 h
Headache Grade 2 (moderate) LOC <1 min or PTA >30 min <24 h or
Poor concentration PCSS >24 h <7 days
Dizziness Grade 3 (severe) LOC ⭓1 min or PTA ⭓24 h or PCSS >7 days
Irritability LOC=loss of consciousness; PTA=post-traumatic amnesia (anterograde/retrograde);
PCSS=post-concussion signs/symptoms other than amnesia.
Ringing in the ears
Drowsiness
Memory problems concussion severity should not be made on the day of
Sadness injury. At present, all concussion severity guidelines, with
Excessive sleep
the exception of the evidence based revised Cantu
guidelines (table),16 grade concussion severity on the day of
Nausea
injury. Most grading scales have placed emphasis on the
Sensitivity to light
presence or absence of loss of consciousness and amnesia.
Fatigue
Supporting this, prospective studies by Collins,10 Lovell,13
Nervousness and Erlanger11 have shown that memory dysfunction
Sensitivity to noise correlates with abnormal neuropsychological test scores
Feeling “in a fog” 48 h after an injury. However, it is also quite clear from the
Numbness/tingling National Football League Concussion Study17 of athletes
Trouble falling asleep who had symptoms and were out of play for more than
Feeling “slowed down” 7 days, as well as from the National Collegiate Athletic
Poor balance Association (NCAA) experience12 of athletes who had
Vomiting symptoms for more than 7 days, that it is important to
monitor all postconcussion symptoms both for severity
and duration. On the day of a concussive injury, one does
neuronal, chemical, or neuroelectrical changes without not know the duration of postconcussion symptoms that
structural change. We now know that structural damage the athlete may experience, and therefore a final grading of
with loss of brain cells does occur with some concussions. the severity of concussion should be deferred until one
In the past decade, the neurobiology of cerebral knows when the symptoms have cleared. It is this belief
concussion has been studied in rodent models. that gave rise to the grading scale shown in the table, in
Concussive brain injury has been shown to trigger a which the most mild grade of concussion has a resolution
pathophysiological sequence characterised by an of post-traumatic amnesia symptoms within 30 min, other
indiscriminate release of excitatory amino acids, massive symptoms within 24 h, and no loss of consciousness. An
ionic flux, and a brief period of hyperglycolysis, followed intermediate concussion is defined as loss of consciousness
by persistent metabolic instability, mitochondrial for less than 1 min, post-traumatic amnesia of greater than
dysfunction, diminished cerebral glucose metabolism, 30 min but less than 24 h, or other postconcussion
reduced cerebral blood flow, and altered neuro- symptoms that last longer than 24 h but less than 7 days. A
transmission. These events culminate in axonal injury and severe concussion occurs when consciousness is lost for
neuronal dysfunction, which clinically may manifest as more than 1 min, post-traumatic amnesia lasts for more
neurological deficits, cognitive impairment, and somatic than 24 h, or other postconcussion symptoms last longer
symptoms (panel). In animal models, this complex cascade than 7 days.
of ionic, metabolic, and physiological events that can In the NCAA concussion study,12 most individuals that
adversely affect cerebral function has been shown to last were graded as grade 3 (severe concussions) by this
typically for less than a week, but can last longer. Exactly concussion grading guideline were given this grading
how long these events last in human beings has yet to be because of concussion symptoms that lasted for more than
determined. It is the lack of a test in human beings to 7 days or post-traumatic amnesia symptoms that lasted
measure these disturbances that makes it difficult to longer than 24 h. Almost no athletes had a period of
accurately grade the severity of a concussion and know unconsciousness greater than 1 min.
with absolute certainty when it is safe to allow an athlete to
return to collision activities. Neurological problems in breath-hold diving
When I initially proposed a grading scale for Massimo Ferrigno, Department of Anesthesiology,
concussion severity and return to play guidelines in 1986,9 Perioperative and Pain Medicine, Brigham and
there were virtually no prospective studies on concussion. Women’s Hospital and Harvard Medical School,
Fortunately, because of several studies in the past Boston, USA
10 years,10–15 we now have a better understanding of the Snorkelling and breath-hold diving are enjoyed by millions
grading of concussion and, to a lesser extent, when it is safe of people around the world. Although most people dive to a
to allow an athlete to return to competition after a few meters below the surface for less than 1 min at a time,
concussive brain injury. Definitive judgement of dives to depths of 30 m or more, lasting 1–2 mins, are

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 Sports neurology
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A different mechanism causes the breath-hold diver’s

hypoxia of ascent: as the ambient pressure surrounding the
diver’s chest rapidly drops during ascent from depth, the
alveolar PO2, and consequently the arterial PO2, also drop
dramatically, particularly close to the surface and this may
cause loss of consciousness. PAO2 values around
30 mm Hg—measured at the end of 45 s working dives to
11 m by Korean Amas18 and of an assisted 150 s dive to 70 m
by an elite diver—attest to this risk.19 At this dangerous
time, the diver may experience a paradoxical relief from air
hunger owing to expansion of the chest wall and the
concomitant fall in alveolar PCO2. Other conditions could
also cause decreased alertness in breath-hold divers. For
example, CO2 buildup from repetitive dives separated by
Rights were not granted to include this very short surface intervals, which do not allow elimination
of CO2 accumulated during each dive, in the absence of
image in electronic media. Please refer hyperventilation. Other mechanisms include the occurrence
to the printed journal. of extreme bradycardia and cardiac arrhythmias: prolonged
R-R intervals, as long as 7·2 s, and various disturbances of
heart rhythm have been observed in human breath-hold
divers, particularly in cold water.20
Decompression illness is caused by formation of bubbles
in blood or tissue from dissolved inert gas during ascent,
and it is typical of diving while breathing compressed gases
(air or other breathing mixtures). However, neurological
Alexis Rosenfeld/Science Photo Library

manifestations suggestive of this syndrome have also been

observed in breath-hold divers. In 1965, Cross21 described
several neurological symptoms including “partial or
complete paralysis, vertigo, loss of consciousness and even
death” in pearl divers from the Tuamotu Archipelago,
where these problems were referred to as “Taravana” (tara,
to fall; vana, crazily). These divers did frequent 1–1·5 min
Figure 3. Some elite breath-hold divers can reach great depths.
dives to 30 m or more with brief intervals between dives,
and dived for about 6 h a day. This pattern of repetitive
breath-hold diving was thought to lead to enough nitrogen
routine for spear-fishermen during competitions. There are accumulation to cause decompression problems. In the
also a few elite breath-hold divers (figure 3) who constantly same year, similar neurological problems were also
try to outdo each other in order to establish depth records, described in four divers from the Danish Navy after
which have recently exceeded 150 m. These deep record repeated breath-hold dives to 15–20 m.22 The fact that these
dives typically last 3–3·5 min, with very rapid descent and divers were successfully treated with recompression in a
ascent made possible by a weight and a buoyancy balloon, hyperbaric chamber supports the notion that these were
respectively. Breath-hold divers face various neurological indeed cases of decompression illness.
problems related to their diving practices. After a long time interval without any more reports of
A decrease in, or even loss of, consciousness from hypoxia decompression illness in breath-hold divers, serious
can occur in breath-hold divers as a consequence of forceful neurological problems—including sensory, motor, visual,
hyperventilation or ascent from a prolonged dive. and speech disturbances—have recently been described in
Hyperventilation before a dive is very effective in decreasing divers from Australia,23 Japan,24,25 Italy,26 Spain,27,28 and
the CO2 stores in the diver’s body; therefore it will take longer France.29 Typically, most of these neurological problems
for enough CO2 to accumulate to force the diver to resume resolved either spontaneously over a few hours or were
breathing. Unfortunately, hyperventilation only minimally successfully treated with recompression. Reappearance of
increases the oxygen stores of the diver, who therefore can slip decompression illness among breath-hold divers may have
into hypoxic syncope before feeling the urge to breathe. If this been brought about by changes in diving techniques; for
occurs in water and the diver is alone, he or she will drown. example, all the Spanish divers had repeatedly dived to 40 m
Generalised weakness, sometimes followed by loss of or more using electrically operated underwater scooters. In
consciousness, is sometimes seen in swimming pools during the case of the Ama divers from Japan, who do a large
competitions of breath-hold duration at rest. These number of breath-hold dives to less than 25 m and of about
competitions, where hyperventilation is routinely practiced 1 min in duration, the recent introduction of wetsuits has
and breath-holds can last for more than 5 min, have recently allowed longer daily diving sessions. This carries the risk of
become quite popular in several countries. decompression illness, which had not been previously

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For personal use. Only reproduce with permission The Lancet Publishing Group.
 Forum Sports neurology

3 Noakes T, Jakoet I. Spinal cord injuries in rugby union players. BMJ 1995; 310: 1345–46.
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