Can high school football players develop Traumatic brain injury without a concussion

note:This a reposting of a commentary posted five years ago. So few people saw the post I am offering it again as High School Football season is underway and subconcussive head blows occur every Friday night. 

Traumatic brain injury (TBI) is classified as mild,moderate and severe based on mental status change and duration of loss of consciousness (LOC). Mild TBI  involves LOC less than 30 minutes and corresponds to  a Glascow Coma Scale rating of 13-15. For example, a football player who appears stunned and confused with only brief of no loss of consciousness would have a Glascow score of 14.

A major element of TBI is diffuse axonal injury thought to be caused by rotational and linear acceleration of the brain. Conventional MR imaging and CT images do not detect that type of changes. However, diffusion tensor imaging (DTI) can detect changes in fiber tracts reflecting changes in diffusion of water into nerve tissues.A DTI based measurement ,fractional anisotropy (FA) ,reflects water movement along the axons.In normal tissue FA is high ( approaches 1)

DTI abnormalities have been demonstrated in concussive cases of  mild TBI and the degree of abnormality correlates with the severity of post trauma symptoms.(see here). Typically FA increases acutely in TBI and later on values are decreased (see here ), although there is some inconsistency about the direction of change in this measurement  in the literature and there are case reports in which acutely FA decreases.

Football players  college,high school and professional, who have sustained concussions,have been shown to have abnormal DTIs.

There are  several publications  (1. Davenport et al,2.Talavage,3.Barzarian  4.McAllister )describing research involving college and high school football players that have shown similar DTI changes in athletes who did not have clinical concussions,These imaging changes seem related to multiple sub-concussive head blows.Some studies-but not all- have also shown that these DTI findings correlate with decrements in memory test results over the course of one season.Generally these DTI abnormalities correlate with measurements of acceleration forces of the skull detected by in- helmet accelerometers.

 1)EM Davenport and her colleagues from Wake Forest studied the cumulative effects of head impacts in a single high school football season in players without a recognized concussion.(Abnormal white matter integrity related to head impact exposure in a season of high school varsity football" J of Neurotrauma 2014 Jul 14, published ahead of print).

The authors' summary:

"We show that a single season of football can produce MRI measurable brain changes that have been previously associated with mTBI (mild TBI) .Finally, we demonstrate that these impact related changes in the brain have a strong association with postseason change in cognitive function." The cognitive function was noted in a verbal memory composite score which correlated with the magnitude of the MR findings.

 2) TM Talavage and coworkers studied 11 high school players with functional MRs (fMR),measures of head impact events and neurocognitive function testing. "Functionally detected cognitive impairments in high school football players without clinically diagnosed concussion." J of Neurotrauma. 31:327-338,Feb 2014)

 Unlike most of imaging studies of TBI this group found abnormalities in the frontal lobe with functional MR.DTI was not done.

 Quoting from the authors summary:

"Additionally, we observed players in a previously undiscovered third category, who exhibited no clinically-observed symptoms associated with concussion, but who demonstrated measurable neurocognitive (primarily visual working memory) and neurophysiological (altered activation in the dorsolateral prefrontal cortex [DLPFC])."

3 JJ Bazarian  studied 10 college football players over the course of one season. ( "Persistent Long Term cerebral White Matter Changes after Sports related Repetitive Head Impacts. Plos one 9(4),e94737)

 Head impacts were recorded and measured by helmet accelerometers and DTI was done preseason, immediately post season and six months after the end of the season.

 DTI abnormalities in white matter were noted in these players none of whom sustained a clinically evident concussion. The changes in most players,but not all, were also seen in the six month followup images. .. There was a positive  correlation between number of head impacts and DTI findings. The DTI changes were not correlated with changes in cognitive testing or tests of balance.

4)  TW McAllister's study involved 80 college football and hockey players ( "Effect of head impact of diffusivity measures in a cohort of collegiate contact sports athletes", Neurol. 10:1212/01Dec 11 2013.)

Quoting the authors:

"The magnitude of  [TDI] change in corpus callosum MD (mean diffusivity) was associated with poorer performance on a measure of verbal learning and memory."  Again these findings occurred in players with no recognized concussions.

The risk of concussion is greater in certain positions such as quarterback and wide receivers. Lineman , on the other hand have fewer concussions but most experience multiple head impacts during each game and each full contact practice session.See here for a detailed study on impact forces on various player positions.

Maugans and coworkers studied athletes younger than typical varsity high school players.These players were 12 to 15 years of age and DTI scans done fairly soon after the concussion did not show abnormalities in diffusion indicators including fractional anisotropy.

Dementia Pugilistica as a clinical condition in professional boxers was described as a clinical entity in a JAMA article in 1928.In 1973 the pathological findings were published. In 2005,Omalu et al published the results of an autopsy on an National Football League  player, Pittsburgh Steeler center,Mike Webster, on whom Dr. Omalu had performed an autopsy 3 yearns earlier.This was the first report of Chronic Traumatic Encephalopathy in a football player.

Zhang et al provided some data regarding brain changes in boxers who were symptoms free and who had a normal neurological exam. 47 professional boxers ( age 30 +/-4.5 years ) underwent conventional MRIs and DTIs.In 42 the conventional MRI was normal while 7 demonstrated some focal non specific white matter changes. The 42 demonstrated abnormal DTIs, with decreased fractional anisotropy in regions of the corpus callosum and internal capsule.Boxers have been the canaries in a coal mine.Their experience has made it clear that repeated blows to head can cause permanent progressive brain damage that is not immediately apparent but develops over a  variably long period of time.The question is to what extent does this apply to football in which the players wear helmets.For years it was believed that helmets were adequately protective but now that view is increasingly less plausible.

By 2013 the NFL agreed to settle a class action law suit brought about by former NFL players and their families  but the judge did not agree to the amount offered..Now the NFL has seemingly admitted that as many as one third of players will develop some sort of cognitive impairment and that they will have funds available to cover the agreement.

The distinction between a concussive and a sub-concussive head blow is on the margin indeterminate.  A player may experience a blow to the head and feel slightly dizzy or dazed and not report those symptoms to the coach or trainer. There may be social or peer pressures on players to not report symptoms as they would be benched and not allowed to play until they complete whatever concussion protocol is in place.So the distinction between a group of players with a concussion and a group with no history of reported concussion is  not one based on clear cut objective criteria,often relying on the voluntary reporting of subjective symptoms.So it should not be surprising that cognitive tests and brain imaging studies show similar findings in football players with and without a concussion history.

So in reply to the title question, yes I believe there is convincing evidence, But there has not yet been established a clear linage between the changes in cognitive tests and brain imaging studies  seen after a season of high school or college football  and the development of  chronic traumatic encephalopathy .