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Repetitive Head Impacts: A Growing Concern in Youth Sports

 

Brain trauma among football players (and athletes in other sports such as soccer and ice hockey) may be less the result of violent collisions that cause concussions as the cumulative  effect of repetitive head impacts (RHI).  The discovery has lead to increased calls by experts to take steps at the youth and high school level to limit exposure to such repetitive trauma, especially to athletes at the youth and high school level playing contact and collision sports, while others urge a more cautious approach until more is known.Pop Warner football

Although scientists have long suspected that RHI caused brain damage, especially in boxers, a 2010 study of high school football players by researchers at Purdue University [1,13] was the first to identify  a completely unexpected and previously unknown category of players who, though they displayed no clinically-observable signs of concussion, were found to have measurable impairment of neurocognitive function (primarily visual working memory) on computerized neurocognitive tests, as well as altered activation in neurophysiologic function on sophisticated brain imaging tests (fMRI). 

Indeed, researchers found, the players with the most impaired visual memory skills were not those in who had been diagnosed with concussions but were in the group which, in the preceding week, had experienced a large number of RHI - around 150 hits - mostly in the 40 to 80 g range.  

Publication of the Purdue study sent shock-waves reverberating through the football world, with the findings cited by concussion experts calling on youth sports organizations to take more aggressive action to minimize exposure to RHI, including sub-concussive blows, by changing the way contact and collision sports are played and practiced, and reducing the amount of brain trauma a child incurs by limiting the number of hits they sustain in a sports season and over the course of a year and a career.  

Pop Warner responded by instituting rule changes in 2012 designed to limit contact during practices.

In 2013, state high school athletic associations in Arizona, Washington State, Iowa, and Texas moved to impose some limits on full-contact practices.  On June 3, 2013, the Pac-12 announced that it would adopt a policy limiting full-contact practices as well, although it did not state what those limits would be, only that they would be less than allowed by the NCAA; other major college football conferences, however, have not followed suit, at least so far.  

On July 7, 2014, the NCAA issued new guidelines recommending that full-contact practices be limited to two per week during the season.  The NCAA guidelines also recommend four contact practices per week during the preseason and no more than eight of the 15 sessions during spring football. 

Just two weeks later, on July 21, 2014, California governor Jerry Brown signed into law AB 2127, limiting middle and high school to two full-contact practices - each no more than 90 minutes long - per a week during the 30 day period before the regular season and during the regular season itself, and banning off-season contact practices completely.   

Cause for concern

Since publication of the Purdue study, similar findings about the effect of RHI, at least in the short-term, have been reported by researchers in a number of other studies [8,9,16,19,21,22], and in one study, [23] even six months after a football season ended. 

In a 2012 study, [8] researchers at the University of Rochester Medical Center (URMC) measured before-and-after data from the brains of a group of nine high school football and hockey players using an advanced form of imaging similar to an MRI called diffusion tensor imaging (DTI).  They found subtle evidence of axonal injury at the cellular level in six athletes who were not diagnosed with concussion but sustained RHI during the normal course of play.  The abnormalities disclosed on post-season DTI scans among the players were closer to the scan of the one player with diagnosed concussion than to the normal brains in the control group. Axons, which are like cables woven throughout brain tissue, swell up when traumatic brain injury occurs.

The imaging changes also strongly correlated with the number of head hits (self-reported by the athletes in a diary), the symptoms experienced, and independent cognitive tests, said lead author Jeffrey Bazarian, M.D., M.P.H., associate professor of Emergency Medicine at URMC. 

Another 2012 study [19] found that new learning on a sophisticated pencil-and-paper neurocognitive test declined over a single season of RHIs among college football and hockey players who did not experience concussions.  The study found that the players had poorer post-season reaction time and scores on a test of visual attention and task switching, which deficits were associated with greater head impact exposures.  Comparing DTI scans before and after a sport season, the researchers also found a significant increase in 

Using DTI imaging technique, researchers at Indiana University School of Medicine and the Geisel School of Medicine at Dartmouth College, found in a 2013 study [16] significant differences in brain white matter of varsity football and hockey players compared with a group of non-contact-sport athletes, with the number of times they were hit correlated with changes in the white matter. They also found that some of the athletes, none of whom suffered diagnosed concussions, didn't do as well as predicted on tests of learning and memory at the end of the season, although the study did not find "large-scale, systemic differences" in the brain scan measures, which the authors found "somewhat reassuring" and consistent with the fact that millions of athletes play contact sports for many years without developing progressive neurodegenerative disorders.[17,18]

Another 2013 study by researchers at URMC and the Cleveland Clinic [9] also found evidence of brain damage in college football players from RHI in the form of elevated levels of S100B, a protein in the blood usually present only in the brain. The presence of the S100B protein triggers the release by the body of antibodies which can then leak back into the brain through the damaged blood-brain barrier, where they are thought to attack brain tissue.  The highest protein levels were found among players who sustained the most hits to the head during games and practices.   

The findings of these studies support anecdotal evidence from other studies that football players not diagnosed with concussions nevertheless seem to suffer cognitive impairment. In other words, some players are injured, but don't know it (unlike players who know they are experiencing concussion symptoms but who, for a variety of reasons, fail to report such symptoms, a problem which continues to be chronic in contact and collision sports). 

Changes to brain persist

Perhaps most concerning, a 2014 study by Bazarian and his URMC colleagues [23] found changes in brain white matter in a small group of college football players which persisted six months after the season was over. They found a strong correlation between the white matter changes and the number of head hits with a peak rotational acceleration exceeding 4500 rad/sec2 and the number of head hits with a peak rotational acceleration exceeding 6,000 rad/sec2, and an especially strong correlation where the number of the former exceeded 30-40 for the season, and the number of the latter exceeded 10-15 for the season. (For reference, a person nodding his head up and down as fast as possible produces a rotational acceleration of approximately 180 rads/sec2).

That six months off may not be long enough for the brains of football players to completely heal after a single season, putting them at even greater risk of head injury the next season, was concerning, said Bazarian.

"I don't want to be an alarmist, but this is something to be concerned about.  At this point we don't know the implications, but there is a valid concern that six months of no-contact rest may not be enough for some players," he said. "And the reality of high school, college and professional athletics is that most players don't actually rest during the off-season. They continue to train and push themselves and prepare for the next season."  

Troubling findings 

The findings of the 2010 Purdue study alone were troubling, said Larry J. Leverenz, PhD, ATC, a Clinical Professor in the school's Department of Health and Kinesiology, shortly after the study was published, because it meant that players were:

  1. Escaping detection.  Because they have not suffered damage to areas of the brain associated with language and auditory processing, they are unlikely to exhibit clinical signs of head injury (such as headache or dizziness), or show impairment on sideline assessment for concussion, all of which test for verbal, not visual memory, Leverenz said that "there is no way right now to identify" the group suffering sub-concussive blows to the head that may be dangerous.  Hence, they will likely continue participating in football-related activities, even when changes in brain physiology are present, which studies show likely increases the risk of future neurologic injury;
  2. Didn't know they were injured.  If working memory deficits are sufficiently small, a player may not be aware of the additional effort required to complete everyday tasks, and therefore not think to bring the problem to anyone's attention (although at least one of the players in the impaired group seemed to have figured this out, and played with better, heads-up technique the next season, reducing the number of hits he took to the forehead); and
  3. Facing an uncertain future.  Even though the players in the Purdue study who suffered short-term cognitive impairment from repeated sub-concussive blows exhibited results on fMRI and ImPACT tests administered before season #2 comparable to the baseline results before season #1, their return to baseline does not necessarily mean that there was 100% recovery.  It is possible that the damage will only be known over the long term, years later.

Commenting at the time on the Purdue study for Sports Illustrated [15], Randall Benson, a neurologist at Wayne State University in Detroit, speculated that the Purdue researchers may have taken what amounted to a "real-time snapshot" of the early stages of the corrosive creep that wears away at the frontal lobe, a part of the brain involved in navigating social situations. Too much erosion and victims reach a breaking point - like former Steelers offensive lineman Terry Long, who died in 2005 from drinking antifreeze. "It's an insidious progression," Benson said, "and it's not obvious when you talk to [players]."

Four years later, Benson's speculation was echoed in eerily similar comments by Bazarian and his colleagues in the 2014 URMC study: "[i]f RHIs are related to neurodegeneration many years later, a long clinically silent period between the onset of neuronal injury and overt symptoms of dementia would not be unexpected."  During this clinically silent period, however, there may be indicators of dysfunction on a cellular level, such as the elevated levels of S100B antibody found in the cerebral spinal fluid in the football players in the study, even six months after the end of the season, which he said, could "potentially herald[ ] the early stages of [chronic traumatic encephalopathy] or CTE."

"Pending confirmation in a long term longitudinal study tracking athletes prospectively for years to decades looking for manifestations of early cognitive dysfunction and dementia," writes Bazarian, "we believe our results suggest that these persistent DTI changes are likely detrimental.  If borne out in future research, the long-term persistence of these [white matter] changes would mean that athletes returning to play the following season would be at risk for expanded RHI-related WM changes, undetectable by conventional assessments. Could the lack of WM recovery we observed result in cumulative WM damage with subsequent football seasons of RHI exposures? If so, could
this cumulative WM damage be related to the long-term development of CTE?"

A definitive answer is likely years away. 

Purdue study details 

In a two-year study of high school football players at one Indiana high school, the Purdue researchers were hoping to solve the riddle of why, among players experiencing similar magnitude and number of blows to the head, some sustained concussions and others do not.  To answer the question, the study followed players over the course of two seasons:

  • Pre-Season: In the week before "two-a-days" each season, the players (21 the first year, 28 the second, including 16 returning players) took baseline ImPACT tests (a computerized neurocognitive exam of memory and concentration), and underwent functional MRI (fMRI) tests, which measures working memory while their brains were being monitored with magnetic resonance imaging.
  • In-Season
    • Monitored hits: Each player's helmet was equipped with sensors (accelerometers) which relayed dPurdue researchers monitoring hits on sideline of football practiceata on head collisions wirelessly to equipment on the sidelines during each play using a Head Impact Telemetry (HITSTM) system:
      • The 21 players who participated in the study over the course of the season experienced 15,264 "collision events" (a motion/action during which at least one accelerometer registered a magnitude in excess of 14.4 g's of linear force) across 48 practices and games, or an average of 15.5 collision events per player per practice or game; and 
      • Among players who started for either the varsity or junior varsity, per player collision event totals ranged from a high of 1855 (38.6 events per session) to a low of 226 (4.7 events per session).
    • Testing: Of the eleven players invited to undergo "In Season" assessment (ImPACT and fMRI testing), three had been diagnosed by the team physician with concussion, and eight had accrued an unusually large number of helmet collisions (150+, mostly in the 40 to 80 g range of linear force) or at least one high magnitude acceleration (more than 80g of force) during that week's practices and games.
  • Post-Season: 10 of the 11 players who underwent In-Season assessment then returned 1-3 months after the season for "Post-Season" assessment (ImPACT and fMRI testing).

Comparing pre-season and in-season test results, the researchers found that players fell into three groups:

  1. Four who demonstrated no impairment/no change in neurological behavior comparing pre-season/in-season;
  2. Three who exhibited signs and symptoms of concussion and a clinical diagnosis of concussion, which neurological impairment was subsequently confirmed in neurocognitive (ImPACT) and fMRI tests; and
  3. Four who exhibited no symptoms of concussion but who nevertheless were found to have statistically significant reductions in their ImPACT scores for verbal and/or visual memory and significantly decreased fMRI activation levels in regions of the brain strongly associated with working memory.  fMRIs of cognitively impaired football players

The third group constituted a completely unexpected and previously unknown category of players who, though they displayed no clinically-observable signs of concussion, nevertheless showed measurable impairment of neurocognitive function (primarily visual working memory) on neurocognitive tests, as well as altered activation in neurophysiologic function on sophisticated brain imaging tests (fMRI). 

Indeed, researchers found, the players with the most impaired visual memory skills were not those in the concussed group but from the group which, in the preceding week, had experienced a large number of subconcussive hits - around 150 hits - mostly in the 40 to 80 g range. 

The Purdue researchers suspect that the functionally, but not clinically impaired group comprise players who experienced neurologic trauma arising from repeated, sub-concussive head collision events, each of which likely produces sub-clinical stress on neural tissue in the brain.

More concerning, "these players not only may be representative of the group associated with ‘unreported' concussions, but also are also likely to meet the criterion" for inclusion in a group which, because they suffer repetitive, sub-concussive blows to the head, may be at increased risk of further, long-term brain injury, such as CTE, said the study.

Linemen most at risk

The group of functionally, but not clinically impaired, players were also different from the group of concussed players in a number of important respects:

  • They experienced a significantly higher total number of collision events than any other group;
  • They were primarily linemen, who experienced helmet-to-helmet contact on nearly every play from scrimmage, often to the upper forehead above the facemask. "These are the kids who put their head down and take blow after blow to the top of the head," said Eric Nauman, assistant professor of biomedical engineering and basic medical sciences, who leads Purdue's Human Injury Research and Regenerative Technologies Laboratory. As a Sports Illustrated cover story on the study put it, "It wasn't the rare, excessively violent collision between the wide receiver and the free safety, the Patriot missile intercepting the Scud, that mattered most, but rather the milder, more frequent kind of hits that replicated two adolescent rams knocking heads."  

    The Purdue results are consistent with the findings of a 2010 study of college football players reported in the Journal of Athletic Training [2] that head-impact exposure differed significantly by position, with linemen (both offensive and defensive) and linebackers receiving more impacts per practice and games than other positions, while lineman, linebackers and defensive backs recieved more impacts to the front of the head than the back, with quarterbacks experiencing a higher pecentage of impacts to the back of the head compared with the front; and

  • They experienced more higher magnitude (more than 80g) collision events directed to the top front of the helmet - impacting parts of the brain involved in working memory, including visual working memory, a form of short-term memory for recalling shapes and visual arrangement of objects such as the placement of furniture in a room - while the concussed players tended to take heavy, high velocity hits to the side of the helmet.
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