22 July 2019

Lifting the lid on footballers’ brains

Clinical Neurology Sport

The discovery of chronic traumatic encephalopathy (CTE) in two former rugby league players has hit Australian contact sport hard.

The short paper published last month in Acta Neuropathologica Communications by Associate Professor Michael Buckland, head of neuropathology at Royal Prince Alfred Hospital and the Molecular Neuropathology Program at Sydney University’s Brain and Mind Centre, is quite sparse on details. That’s because it’s not a research study but the report of two coronial cases, and subject to a raft of ethical restrictions.

But it has seized the nation’s attention. Former and current players have responded by pledging their brains to research, and three law firms have flagged class action lawsuits against the National Rugby League – in addition to one long in the works against the Australian Football League – amid a chorus of pleas, warnings and doubts that sport-induced CTE is even a thing.

The codes cannot claim to have been blindsided, given the experience of the US’s National Football League, which has been dealing for decades with the spectre of neurodegeneration due to repeated head traumas.

Since facing legal action from 4500 players, the NFL has paid out close to A$1 billion in concussion settlements and in 2016 formally acknowledged a link between American football and CTE.

First documented in 1928 in boxers, and called punch drunk syndrome or dementia pugilistica, the condition is well enough recognised to have entered the language: when a boxer spouts some words of not-quite-wisdom, do we not mutter: “Hmmm, someone took a few too many knocks to the head”?

And yet the science behind this 90-year-old diagnosis is still controversial. But is it a genuine controversy, or a virtual certainty that vested interests are trying to keep at bay for as long as possible?

Boston University is the institution at the forefront of CTE research, with a dedicated centre and a brain bank. Its researchers define the condition as “a progressive neurodegeneration characterised by the widespread deposition of hyperphosphorylated tau (p-tau) as neurofibrillary tangles” around blood vessels and at the depths of cerebral sulci. Clinical symptoms include irritability, aggression, depression, dementia, motor problems and parkinsonism.

A 2013 paper by Robert Stern and BU colleagues for the American Academy of Neurology claims to have found two presentations of CTE: early onset with mood and behaviour features, and later onset with cognitive and motor features.

Everyone so far diagnosed with CTE has a history of repeated minor traumatic brain injury.

Since it can only be definitively diagnosed post-mortem, and the brains made available for analysis have been mostly those volunteered by former sportspeople suffering from mental health problems, there is an obvious question of selection bias.

CTE sceptics say its features can be explained by other dementias, ageing and drug and alcohol use.

It’s a further difficulty that in late stages, both the clinical presentation and the pathology of CTE resemble those of Alzheimers.

Asked about its official stance on CTE, the AFL’s head of health, safety and laws Patrick Clifton tells The Medical Republic it “accepts that neurodegenerative disease can be associated with head trauma. The AFL has been investing in changes to rules to protect the head, reporting processes and research for over two decades.”

He says the league spends $250,000-$350,000 a year on short- and long-term concussion research projects. 

But as The Herald Sun has reported, that money all comes from player fines, not the AFL coffers.

The NRL is more guarded: “The NRL’s approach to the management of head injuries is based on global best practice. The NRL has significantly increased its focus and investment in this area of player safety and will continue as an active participant in the work of the global sport community to advance the understanding and management of head injuries in contact sport.  

“The findings released will be reviewed by the NRL before any further comment is made.”

As far as concussions go, there is no doubt that the codes have become hypervigilant over the past decade, with new technology to monitor head knocks, on-field assessment criteria and return-to-play rules.

The rise of women’s competitions in collision sport is also heightening the awareness, as women appear more likely to suffer, and perhaps also to report, concussions.

Defined as traumatic brain injury causing short-term neurological impairment, concussion can be elusive enough even in the immediate term. The SCAT5 on-field assessment tool looks for 22 subtle and non-specific symptoms beyond the classic one of falling like a pancake on the field. But most people recover completely from concussion within three weeks, usually much sooner, with rest.

There is such a thing as post-concussion syndrome, which lasts longer, and second-impact syndrome, which involves a fresh blow within the recovery period and can cause catastrophic brain damage or death.

But those are rare enough that the new vigilance around concussions implies a tacit acknowledgment of long-term consequences, of a kind we all dread more than any transitory symptoms: losing control of our minds, memory and mood as we age.

Before the two studied by Professor Buckland, the only other Australian former sportsman with brain pathology meeting CTE criteria was rugby player Barry “Tizza” Taylor. His son Steve Taylor wrote a moving account of his father’s sad decline into memory loss, fits of rage and paranoia for the June 30 Sun-Herald newspaper, with a plea to recognise the reality of CTE.

But in the same edition of the paper, World Rugby chief medical officer Dr Martin Raftery threw doubt on the Buckland diagnosis. He cited studies saying the agreed upon CTE neuropathology could be explained by ageing, drug use or other neurodegenerative diseases and that there was insufficient evidence that sports concussion led to CTE.

The Concussion in Sport Australia position statement released in February by the Australian Institute of Sport, Australian Medical Association, Australasian College of Sport and Exercise Physicians and Sports Medicine Australia, takes a hard line on concussions, with the mantra: If in doubt, sit them out.

But the statement says there is “currently no reliable evidence clearly linking sport-related concussion with [CTE], a condition with unclear clinical diagnostic criteria. The evidence … consists of case reports, case series, and retrospective and post-mortem analyses.

“Due to the nature of the studies, and the reliance on retired athletes volunteering for an autopsy diagnosis, there is significant selection bias in many of the reports. The studies to date have not adequately controlled for the potential contribution of confounding variables such as alcohol abuse, drug abuse, genetic predisposition and psychiatric illness.”

The name Paul McCrory comes up in every story on this subject, even though he doesn’t speak to the media, because he is the loudest denier of the diagnosis of CTE. An associate professor at Melbourne University’s Florey Institute of Neuroscience and Mental Health, he chairs the International Consensus Conference on Concussion in Sport and heads the AFL Concussion Working Group. The former Collingwood club doctor has also consulted to the NFL and the NRL, and co-authored the research cited by Dr Raftery.

He makes his scepticism about CTE clear in a 2016 talk available on YouTube titled “The Concussion ‘Crisis’ – Media, Myths and Medicine”, and suggests media reporting has driven children out of sport.

But it’s not only Big Sport-affiliated doctors and academics who have drawn attention to the holes in the evidence.

In 2015, Joseph C. Maroon et al., in a systematic review published in PLOS One, note the clinical and neuropathological overlap of CTE with other neurodegenerative diseases and say the reporting of CTE has “led to widespread speculation far beyond the conclusions that can be drawn based on the current state of CTE research”.

Christopher Randolph, clinical professor of neurology at Loyola University Medical Centre in Chicago, makes a more forceful case in a 2018 article in the Archives of Clinical Neuropsychology titled “Chronic traumatic encephalopathy is not a real disease”.

He asserts that “traumatic brain injury does not cause neurodegeneration, protein deposits in the brain are a poor predictor of behavioral symptoms, p-tau is not necessarily toxic or self-propagating, and retired NFL players are actually much physically and mentally healthier than men of their demographic background”.

He even warns that the media hype over CTE in the past decade might be responsible for a rise in suicide rates among retired players, who might have a treatable condition such as depression, but now believe they have an irreversible progressive disease, “and chose the path of suicide as a result”.

Professor Randolph declined to comment further to The Medical Republic.

It’s true that the nature of the studies so far does not allow estimates of the incidence or prevalence of CTE, let alone prove a causal link between repeated episodes of brain trauma and neurodegeneration, and that so far no mechanism can account for how one becomes, promotes or causes the other.

But there’s no doubt in the mind of neurophysiologist and concussion specialist Alan Pearce, an associate professor at La Trobe University and the research manager of the Victorian arm of the Australian Sports Brain Bank, which was founded last year in Sydney by Professor Buckland.

CTE is “definitely” a distinct disease, he says, with different tau patterning from other dementias such as Alzheimers (though in later stages they become indistinguishable) and frontotemporal lobar degeneration, and a clear association with a history of head trauma.

He’s hoping more people with such histories but no symptoms will donate their brains, to help tease out more answers while countering the selection bias.

“If you have a history of concussions but no ongoing problems, that’s great – that’s what we need to compare with the footballers who are struggling with mental health issues, balance, memory,” he tells The Medical Republic.

“It’s just as important for people with no symptoms to donate. Their contribution would almost be greater, because we need to understand the rate of CTE, why are some people getting it and not others if that’s the case, and whether there’s a threshold for tau in the brain where we start to see problems.”

Professor Pearce uses transcranial magnetic stimulation to detect neurophysiological changes in people with a history of concussion and head trauma. He began using TMS about 25 years ago to study what is now known as neuroplasticity, and acquired an interest in brain injury. This led him to start looking at concussion in Australian Rules footballers about a decade ago, at a time when it was regarded as an American issue.

“I started to try to understand if there were any differences between older footballers with cognitive and motor problems with a history of head traumas and concussions compared to people of the same age who’d never played,” he says. “I was able to see differences in the functioning of the brain that seemed to correlate with slowing of reaction times, fine motor control problems, memory and attention issues in cognitive testing.”

He published two papers in 2014 in which TMS revealed increased corticospinal inhibition or “braking” in brain processes after concussion that might explain the players’ self-reported symptoms.

“They were thinking, you’re just getting old, but when you’ve got guys in their late 40s and 50s presenting with issues you’d expect of a 70-year-old, it seemed to be indicative of accelerated ageing,” Professor Pearce says.

He hopes his research on live subjects will eventually dovetail with the post-mortem brain analyses of Professor Buckland.

He is not currently working with a big sporting code. After the 2014 papers he was approached by the AFL, which offered him funding to continue the work, but then tied his hands, in an odd saga covered at length by Wendy Carlisle in The Monthly last September.

“At the start – maybe I was naïve – I thought they were in good faith; but a year into it, I started to think there’s something going on,” he says.

First the AFL insisted on recruiting the players for him, which raised a red flag about sampling bias. Then, after 18 months, during which he tested dozens of umpires as controls, the AFL had still sent him no subjects. Then when he secured eight participants out of a list supplied by the AFL, the organisation wouldn’t let him also perform the cognitive and motor testing that gave crucial context to the TMS results.

“I lost the argument on that one and my research ended up being useless and unusable,” he says.

It got weirder. “In the week before the end of the contract I got an email [from two AFL employees] saying they were concerned about the numbers tested to date and the lack of data with only TMS. I said, ‘Don’t you remember our conversation? This is a concern I have brought up with you many times. Can we meet?’ And I got no response. And I felt they were starting to protect themselves.”

The AFL says it does not accept Professor  Pearce’s description of the relationship. 

“The AFL supported Professor Pearce’s work financially and by encouraging past player participation but reasonably prioritised clinical activities with validated outcomes for those past players before any research projects,” Mr Clifton says.

“Alan Pearce decided to not continue after two years – that was his choice.”

Since then, Professor Pearce has worked with retired professional rugby league players, who have all come to him through word of mouth without NRL involvement, and found similar neurophysiological correlates for cognitive and motor changes decades after their last concussions.

He says it’s hard to have confidence in statements about concussion and CTE that are backed by “Big Sport”.

“Sport Australia says you’ve got to be aware of concussions and manage them properly, but that the link between repeated head traumas and concussions and CTE is ‘tenuous’. Well, you can’t have it both ways. Make sure they don’t get concussed and have a graduated return to play, but long term don’t worry about it?”

Former AFL player manager Peter Jess has come to the same certainty about CTE from the opposite direction, having worked with large numbers of players and watched them change during and after their careers.

“The incontrovertible truth is that repetitive collisions cause long-term neurological damage, and it’s something we’ve known for a long time,” he tells The Medical Republic.

Mr Jess has had a class action lawsuit in the works against the AFL for many months and expects it will be filed soon. He says after the obligatory seven named plaintiffs, who are ready to proceed, the class theoretically expands to include every former AFL/VFL player, or about 6500 people.

“Each player is unique in terms of damage,” Mr Jess says.

“Some present purely behavioural, some are structural, but they’re all symptomatic. One had a scan that showed 11 lesions on his brain – he’s gone through the phase of mood and behaviour disorders and he’s into cognition disorders and will move into motor-skill problems.

“We say the AFL has known [at least since the landmark Corsellis et al. paper of 1973] that there was a likelihood of every participant having a possibility of long-term neurological impairments from playing a collision-based sport.”

He says the claimants’ preferred option “is to sit down and create a paradigm for evaluation, assessment and if there’s a causal relationship explore a compensation scheme”. But the AFL’s attitude was “clearly adversarial”.

“They’ve had 45 years to get this right. If they had a proper workers’ compensation system there’d be enough money to deal with this.”

Besides compensation, he doesn’t believe the AFL has done enough to mitigate the risks on the field.

“We have a game that has no offside, so you’re allowed tackle from 360 degrees,” he says. “We know the major collisions are where people are unsighted. We need to look at the biomechanics of the game and think how we mitigate the collisions, get rid of the scrums because that’s where most of the damage happens.

“There is no agreed protocol for subclinical concussions. That’s the most dangerous part of our sport. You’ve got a large number of players who’ve retired, not because of a catastrophic event but because of an accumulation of subconcussive events – Sam Shaw, Koby Stevens, Justin Clarke, Matt Maguire, Leigh Adams, Jack Fitzpatrick, Jack Frost, Liam Picken and Paddy McCartin.”

St Kilda legend Nicky Winmar, one of Mr Jess’s clients, is also reported to be suffering with mood swings, anger and memory loss and to have considered joining the lawsuit.

“I’m not about stopping people playing sport, I just want it safe,” Mr Jess says.

“We have young men who are seriously impaired by playing football.

“I’d like a dollar for every time I hear that phrase ‘he’s taken too many knocks to the head’ at a past player function, where someone can’t find his car keys or his car – that’s real-world stuff.”

The outspoken Mr Jess compares “Big Sport” to “Big Tobacco” and “Big Alcohol”, calls Professor McCrory and AIS chief David Hughes flat-earthers, and says the SCAT5 assessment tool is more befitting a witch doctor than a club doctor.

“I’ve acted for 1000 people in footy and I see them as 19-year-olds, then I see them as 55-year-olds, and I talk to their wives and they say: this is not the person I married. These people have changed. And those changes are neurological, physical, emotional and psychological.

“They don’t know that they’re damaged, but their wives and families do. Get McCrory and Hughes to visit those guys and tell them it’s transitory and they’ll get better.”

AMA president Dr Tony Bartone says the association recognises that the case for CTE is building, but is reluctant to comment on whether the medical evidence will favour the AFL and NRL class actions, should they make it to court.

“There’s still a lot to learn about it but there’s important growing evidence about the role of repeated low-grade trauma to the head in contact sports, so we need to understand that better and have protocols to manage, even at the most junior and amateur of levels, those accidental ongoing knocks … both in the initial instance and the longer-term complications.

“The AIS is leading this and the codes need to work with the institute and collaborate. I know there are studies going on in academia so everyone needs to work together and keep each other informed. The evidence needs to be shared regularly.

“Sport still remains an important part of growing up, physical development and overall health. But we need to ensure this healthy activity is done in a safe and appropriate manner.”

We’ll have to wait and see if a welter of compensation payments or rule changes result from this combination of cool-headed research and emotive court cases.

What’s certain is that the more time you spend with this subject, the harder it is to watch those powerful, brutal clashes on the field without wincing.

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Grant Holloway
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4 months 18 days ago
Posted by TMR on behalf of Dr Lou Lewis Having been involved in the sport of boxing for 50 years I feel that I am qualified to comment on this article (Lifting the lid on footballers’ brains by Penny Durham 22/7/19) regarding CTE and head injury. Firstly, let me state the obvious, namely, boxing is a dangerous sport! Anyone who tells you otherwise is living in cuckoo land. However, after having read this article regarding football and head injury and brain damage, I realise that there are a lot of people who do live in cuckoo land when they say… Read more »
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