Brain trauma among football players may be less the result of violent helmet-on-helmet collisions that cause concussions as the accumulation of sub-concussive blows.  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.

A 2010 study of high school football players by researchers at Purdue University (1) identified a completely unexpected and previously unknown category of players who, though they displayed no clinically-observable signs of concussion [1], nevertheless showed measurable impairment of neurocognitive function (primarily visual working memory) on neurocognitive tests [2], 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 subconcussive hits - around 150 hits - mostly in the 40 to 80 g range.  

Publication of the Purdue study sent shock-waves reverberating through the football world, and may have been a factor in decisions by the NFL and the Ivy League to limit the number of full-contact practices.

Most recently, the findings were cited by concussion experts calling on youth sports organizations to take more aggressive action to minimize exposure to repetitive brain trauma, 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 [3] they sustain in a sports season and over the course of a year and a career.  

Pop Warner responded by instituting rule changes [4] in 2012 designed to limit contact during practices, but, as of March 2013, no action has yet been taken at the high school level.

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 [5] 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 data on head collisions wirelessly to equipment on the sidelines during each play using a Head Impact Telemetry (HITS^TM) 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 [1] 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. 

The third group constituted a completely unexpected and previously unknown category of players who, though they displayed no clinically-observable signs of concussion [1], nevertheless showed measurable impairment of neurocognitive function (primarily visual working memory) on neurocognitive tests [2], 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 [6], 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 [7] 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.

Cause for concern

Since publication of the Purdue study, similar findings have been made by researchers at the University of Rochester Medical Center (URMC) (8). In measuring before-and-after data from the brains of a group of nine high school football and hockey players using diffusion tensor imaging (DTI), researchers found subtle evidence of axonal injury at the cellular level among six of athletes who were not diagnosed with concussion but sustained many sub-concussive blows during the normal course of play.  The abnormalities disclosed on post-season DTI scans among the players were closer to the 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. 

A 2013 study by researchers at URMC and the Cleveland Clinic (9) also found evidence of brain damage in college football players from sub-concussive hits in the form of elevated levels of 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 in the Rochester and Purdue 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 [1] but who, for a variety of reasons, fail to report such symptoms, which continues to be a chronic problem). 

The findings are troubling, says Larry J. Leverenz, PhD, ATC, of the Department of Health and Kinesiology at Purdue, because the players:

1. Escape 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 [1] of head injury (such as headache or dizziness), or show impairment on sideline assessment for concussion [8], all of which test for verbal, not visual memory, so "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. Don't know they are 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 [9] the next season, reducing the number of hits he took to the forehead); and
3. Face 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 on the Purdue study for Sports Illustrated [7], Randall Benson, a neurologist at Wayne State University in Detroit, suggested 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]."

Is better detection the answer?

One approach to the problem of sub-concussive blows that escape detection via conventional means is to find new enhanced detection methods: If functional impairment could be detected on the sports sideline, a player, like those exhibiting more obvious concussion signs or complaining of symptoms consistent with concussion, could be removed from play.

As Dr. Leverenz noted, the problem with sideline assessment tools in current use, such as the Standardized Assessment of Concussion (SAC) [10] and the Sports Concussion Assessment Tool 2 (SCAT2) [11], is that they test verbal memory, not the visual memory that he and the Purdue researchers found impaired in the functionally, but not clinically impaired, players who experienced at least short-term neurologic trauma from repeated, sub-concussive hits to the head.

All too often, even hits hard enough to cause an athlete to experience signs of concussion that can be observed by sideline personnel, or which cause the athlete to experience symptoms of concussion, go undetected, either because the signs are simply missed by sideline personnel or because the athlete fails to report them (a 2010 study⁷ of Canadian junior hockey players, for example, found that, for every concussion self-reported by the players or identified by the coaches or on-the-bench medical personnel, physician observers in the stands picked up seven) - a persistent problem that, given the "warrior" mentality and culture of contact and collision sports, is not going to go away any time soon, if ever. 

One way to increase the chances of detection is to install sensors [12] in players' helmets or mouth guards to alert sideline personnel to head impact exposure, either from a single, forceful hit, or from less forceful but repetitive blows, that has the potential to result in brain injury, which helps to identify athletes who should be removed for evaluation on the sports sideline and, if found to have a suspected brain injury, referred for further evaluation and banned from a return to play.⁶ 

Hit limits 

But better detection does nothing to prevent such brain trauma, or at least reduce the risk, in the first place.  No matter how good the technology, no matter how good we get at identifying suspected concussions, the essential problem remains: the hits themselves. 

As a result, experts say, the focus must be on reducing the risk of concussions and sub-concussive brain trauma by reducing exposure to concussive and sub-concussive hits [13] that athletes sustain during contact and collision sports.  

"The challenge," said Bazarian, the author of the Rochester study,⁸ "is to determine whether a critical number of head hits exists above which this type of brain injury appears, and then to get players and coaches to agree to limit play when an athlete approached that number."  

1. Talavage T, Nauman E, Breedlove E, et. al. Functionally-Detected Cognitive Impairment in High School Football Players Without Clinically-Diagnosed Concussion. J Neurotrauma. 2010; DOI: 10.1089/neu.2010.1512.

2.  Crisco JJ, Fiore R, Beckwith JG, et al. Frequency and location of head impact exposures in individual collegiate football players. J. Athl Train 2010;45:549-559.

3. Field M, Collins MW, Lovell MR, Maroon J. Does age play a role in recovery from sports related concussion? A comparison of high school and collegiate athletes. J Pediatr. 2003;414:546-553.

4. Pullela R, Raber J, Pfankuch T. et al. Traumatic injury to the immature brain results in progressive neuronal loss, hyperactivity and delayed cognitive impairments. Dev Neurosci 2006;28:396-409.

5. Stern R, Riley D, Daneshvar D, Nowinski C, Cantu R, McKee A. Long-term Consequences of Repetitive Brain Trauma: Chronic Traumatic Encephalopathy. Phys. Med. & Rehab. 2011;3;S460-S467. DOI:10.1016/j.pmrj.2011.08.008.

6. Greenwald R, Chu J, Beckwith J, Crisco J. A Proposed Method to Reduce Underreporting of Brain Injury in Sports. Clin J Sport Med 2012; 22(2):83-85.

7. Echlin P, Tator C, et al. A prospective study of physician-observed concussions during junior ice hockey: implications for incidence rates.  Neurosurg Focus 2010;29(5):E4.

8. Bazarian JJ, Zhu T, Blyth B, Borrino A, Zhong J.  Subject-specific changes in brain white matter in diffusion tensor imaging after sports-related concussion.  Magnetic Resources Imaging. 2012; 30(2): 171-180.

9. March N, Bazarian JJ, Puvenna V, Janigro M, Ghosh C, et. al. Consequences of Repeated Blood-Brain Barrier Disruption in Football Players. PLoS ONE 2013;8(3): e56805. doi: 10.1371/journal.pone.0056805.  

Posted April 6, 2012; most recently revised March 11, 2013

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