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, while others urge a more cautious approach until more is known.
A 2010 study of high school football players by researchers at Purdue University [1,13] identified 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 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. [Editor's Note: 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].
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  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, and in 2013, state high school athletic associations in Arizona , Washington State , Iowa, and Texas  moved to impose some limits on full-contact practices.
Since publication of the Purdue study, similar findings about the effect of repetittive sub-concussive hits, at least in the short-term, have been reported by researchers in a number of other studies.
In a 2012 study, 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 diffusion tensor imaging (DTI). They 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.
In a 2013 study researchers at Indiana University School of Medicine and the Geisel School of Medicine at Dartmouth College, using the same DTI imaging technique, found 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]
A 2013 study by researchers at URMC and the Cleveland Clinic 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 URMC, Indiana/Dartmouth, Cleveland Clinic, 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  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:
Commenting on the Purdue study for Sports Illustrated , 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]."
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:
Comparing pre-season and in-season test results, the researchers found that players fell into three groups:
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.
The group of functionally, but not clinically impaired, players were also different from the group of concussed players in a number of important respects:
The Purdue results are consistent with the findings of a 2010 study of college football players reported in the Journal of Athletic Training  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
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)  and the Sports Concussion Assessment Tool 2 (SCAT2) , 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 study 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 may be to equip players with impact sensors  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 could help medical staff 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.
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, some experts are urging that the focus be on reducing the risk of concussions and sub-concussive brain trauma by reducing exposure to concussive and sub-concussive hits  that athletes sustain during contact and collision sports.
Limiting or eliminating contact practices in football, for example, would, according to a 2013 study by researchers at the University of Michigan, result in an 18% to 40% reduction in head impacts respectively over the course of a high school football season.
The Michigan study pointed to recent research suggesting that the number of head impacts sustained may play a more important role in putting an athlete at risk of developing CTE than clinically evident concussions. Among them were the Purdue and Rochester studies of athletes in high school and college football [1,8,9,12,13] and ice hockey,  which, as noted above, found subtle changes in cerebral function in the absence of concussion symptoms or clinically measurable cognitive impairment which researchers linked to the volume of head impacts, and a much publicized case-study autopsy of a collegiate football player, Owen Thomas, with no reported history of concussions, which revealed early signs of CTE. 
"If verified," lead author, Steven P. Broglio, PhD, ATC, of Michigan NeuroSport and Director of the NeuroSport Research Laboratory at the University of Michigan, writes, these reports "would support the use of head impact numbers to limit the head trauma volume experienced by an athlete each season."
Broglio recognized that "contact sport athletes appear to be at a greater risk for developing CTE," but was careful to note the absence of studies "indicating the relationship between head impacts, concussions, and other factors (eg. genetic profile) that may trigger the disease pathway."
He described the goal of reducing the overall number of head impacts that high school football players sustain in a season as "logical" and "appealing," but noted that, "until the risk factors for chronic traumatic encephalopathy  (CTE) are better defined by carefully designed and controlled research," and research determines "what the advisable limit to head impact exposure should be," employing contact limits or establishing "hit counts " will remain "educated guesses, at best."
Broglio and his colleagues thus recommended that policymakers proceed with caution in imposing such limits.
Finding a way to reconcile two competing demands - minimizing contact practice in order to reduce the number of concussions sustained in practice and the number of sub-concussive impacts that emerging science suggests may have a deleterious cumulative effect  on a player's cognitive function over the long term, while at the same time maximizing the amount of time in practice learning how to tackle and block without head-to-head contact - time that is needed to maximize the protective effect of proper tackling on the number of head-to-head hits players sustain in game action, which can not only result in concussion, but catastrophic neck and spine injuries - will be difficult.
"As a scientist, I am not in a position to make policy," Broglio told MomsTEAM, but "we can't just reduce [the number of contact practices] without looking at the whole picture. We don't know if 18% means anything, or how much less [in terms of the number of impacts] is meaningful."
If he were making policy, however, Broglio would "lean more towards the cautious side" in limiting contact practices, which is not to say that he doesn't think "that a football program could be successful" with some limits on full-speed contact practices. Pointing to rugby, where players practice tackling without helmets without increased risk of head injury in games, he "didn't necessarily buy" the argument advanced by some experts that limiting contact practices would expose football players to increased injury risk in games. As Broglio writes in the study, however, that view comes with a very important caveat: only if "extra emphasis on the appropriate tackling technique [is] put in place to ensure that the highest level of safety was maintained during games."
While the recent movement to limit full-contact practices is intended to make the game safer, some experts agree with Broglio that caution should be the byword . A March 2013 review of current risk-reduction strategies in the British Journal of Sports Medicine  reminds state high school athletic associations and legislatures that, in enacting rules such as limits on full-contact practices, they "need to carefully consider potential injury 'trade-offs' associated with the implementation of injury-prevention strategies, because every change may have certain advantages and disadvantages. That is, by reducing one risk or danger, additional risks may be created." In other words, as the Michigan study points out, limits on full-contact practices could create additional risk of injury to players because they haven't spent enough time learning to tackle properly.
"The challenge," said Bazarian, the author of the Rochester study, "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."
The science has not yet come close to determining that number.
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.
10. Broglio SP, Martini D, Kasper L, Eckner JT, Kutcher JS. Estimation of Head Impact Exposure in High School Football: Implications for Regulating Contact Practices. Am J Sports Med 2013;20(10). DOI:10.1177/036354651302458 (epub September 3, 2013).
11. Benson B, McIntosh A, Maddocks D, et. al. What are the most effective risk-reduction strategies in sport concussion? Br J Sports Med 2013;47:321-326.
12. Breedlove EL, Robinson M, Talavage TM, et al. Biomechanical correlates of symptomatic and asymptomatic neurophysiological impairment in high school football. J Biomech. 2012;45(7):1265-1272.
13. Talavage TM, Nauman E, Breedlove EL, et al. Functionally-detected cognitive impairment in high school football players without clinically diagnosed concussion. J Neurotrauma. 2013;doi:10.1089/neu.2010.1512 (e-publ April 11, 2013)
14. McKee AC, Stein TD, Nowinski CJ, et al. The spectrum of disease in chronic traumatic encephalopathy. Brain. 2013;136(Pt 1):43-64.
15. David Epstein. The Damage Done: While Concussive Hits Dominate the Debate, A Groundbreaking New Study Suggests That Minor Blows - And There Can Be Hundreds Each Game - Are Just As Traumatic. Sports Illustrated. November 1, 2010 (accessed October 14, 2013 at http://sportsillustrated.cnn.com/vault/article/magazine/MAG1176377/2/ ).
16. McAllister TW, Ford JC, Flashman LA, et al. Effect of head impacts on diffusivity measures in a cohort of collegiate contact sport athletes. Neurology 2013; doi:10.1212/01.wnl.000438220.16190.
17. Savica R, Parisi JE, Wold LE, Josephs KA, Ahlskog JE. High School Football and Risk of Neurodegeneration: A Community-Based Study. Mayo Clin Proc 2012;87(14):335-340.
18. Jordan BD, et al. Head trauma and participation in contact sports as risk factors for Alzheimer's disease. Neurology 1990;40:347.
Posted April 6, 2012; most recently revised January 27, 2014