Impact of Sports-Related Concussions Leading to Dialogue on Interventions

There's nothing subtle about the force of a 250-lb linebacker's tackle, a heavyweight boxer's jab to the head, or a hockey defenseman's full-speed body check into a shuddering fiberglass board. In turn, it's not surprising that the oft-violent nature of football, boxing, hockey and other sports can result in mild traumatic brain injury, or concussion.

What is surprising, however, is that an athlete's response to this type of trauma is defined by subtleties. The severity of post-concussion symptoms do not necessarily respond to the severity of a hit. The extent to which those symptoms persist appears to vary from one athlete to another, as does the cumulative effect of multiple concussions over the course of a player's career. Longer recovery times in female athletes than in their male counterparts suggest gender-based differences in risk factors, with hormones potentially playing a key role.

The more clinicians and researchers learn about sports-related concussion, the more it seems that its effective clinical management is in fact dependent on understanding the subtleties of this extraordinarily complex condition. Since the emphasis on toughness in sports has meant that for decades players experiencing symptoms of neurocognitive dysfunction have felt the need to simply “play through it,” researchers in this area have not had the opportunity to explore these subtleties until very recently, and are still at the point where more questions are being asked than answered.

“Probably 90% of what we've learned, we've learned in the last 5 years. We don't pretend to have all the answers at this point in time,” said Mark Lovell, PhD, division head and director of the sports medicine concussion program at the University of Pittsburgh Medical Center, who has consulted with a number of National Football League and National Hockey League teams.

But with each high-profile case that thrusts sports-related concussion and its potential long-term consequences into the mainstream media spotlight, the need to determine what constitutes appropriate management of post-concussion symptoms only increases.

“There is a sense of concern that we protect athletes from catastrophic problems, and that is a major goal of a lot of the research,” said James Kelly, MD, a visiting professor of neurosurgery at the University of Colorado Health Sciences Center and a co-author of several guidelines for concussion management. “But the debate goes on as to how to really do this.”

A WATERSHED YEAR

In some ways, the effects of concussion have been the worst-kept secret in sports. Many NFL fans will remember the 1994 playoff game in which Dallas Cowboys quarterback Troy Aikman, after his helmet collided with a defensive tackle's knee, famously insisted to trainers that he was not in Texas Stadium on a Sunday afternoon but in his home town of Henrietta, OK, at a Friday night high school game. (The following week, Aikman led the Cowboys to their second consecutive Super Bowl victory over the Buffalo Bills.) Jack Dempsey, Joe Louis, Floyd Patterson and Sugar Ray Robinson are just a few of the professional boxers who went on to develop dementia pugilistica, or chronic traumatic encephalopathy, which has been linked to athletes who have suffered multiple concussions.¹

But a number of developments this year alone have sharpened the mainstream media's focus on sports-related concussion and, in particular, its long-term effects. It began in February, just prior to Super Bowl XLI in Miami, when former New England Patriots linebacker Ted Johnson made public allegations that the Patriots had given him insufficient time to recover from a 2002 concussion before forcing him to return to full-contact practice, during which he suffered a second concussion; those and subsequent concussions, Johnson said, caused the severe depression and substance abuse issues that he has struggled with in recent years.²

In April, at the annual meeting of the American Academy of Neurology, Swedish researchers presented data (published the previous fall) indicating that the repeated blows to the head incurred by amateur boxers (who wear helmets and gloves that are more padded than those of professional boxers) led to elevated levels of biochemical markers of neuronal injury up to 1 week after a match.³

Later that month, University of Pittsburgh forensic neuropathologist Bennet Omalu, MD, MPH, presented findings on his examinations of the brains of 3 deceased former professional football players at a meeting of the Sports Concussion Institute, reporting that brain tissue from each of the 3 demonstrated evidence of chronic traumatic encephalopathy.^4,5 Two of the former players had committed suicide; all 3 had suffered from severe depression.

In the June issue of Medicine & Science in Sports & Exercise, researchers from the University of North Carolina published the results of a survey of former professional football players, which suggested that those who had experienced three or more concussions during a career were three times more likely to have been diagnosed with depression than those who had played concussion-free; depression was 1.5 times more common in those who had suffered one or two concussions than in those with none.⁶ An earlier, similar survey study by the same group suggested a link between recurrent concussion and long-term cognitive impairment.⁷

And in September, Omalu and colleagues at the Waltham, MA-based Sports Legacy Institute found a distribution of neurofibrillary tangles and neutropil threads throughout the neocortex, limbic cortex, subcortical ganglia and brainstem ganglia, consistent with chronic traumatic encephalopathy, in the brain tissue of professional wrestler Chris Benoit, who in June murdered his wife and son before killing himself as well.⁸

Again, the subtleties of these particular examples are not well understood. A handful of neuropathological cases studies and a retrospective survey are no substitute for a randomized controlled trial, and although the Swedish boxing study was more scientifically rigorous, it remains unclear how the observed elevated levels of neurofilament light protein and glial fibrillary acidic protein would be manifest clinically, if at all. But despite its limitations, the body of evidence suggesting long-term negative neurological effects of multiple concussions is difficult to ignore.

“When an injury can alter a person's life, it's not a minimal injury. It's not a mild injury,” said Robert Cantu, MD, chief of neurosurgery service, chairman of the department of surgery, and director of sports medicine service at Emerson Hospital in Concord, MA, who has been a pioneer in developing concussion grading criteria and return-to-play guidelines following concussion.

PREVENT DEFENSE

Ideally, the best way to protect athletes from the effects of concussion would be to prevent the concussion from occurring. That, however, is not likely to be a viable option any time soon. Helmets, despite being highly effective for preventing skull fracture and most subdural hematomas, do not prevent concussion. Football helmets are certified to meet a severity index of 1200 or below, but concussion becomes likely at a severity index of 300.⁹ (A new design called the Xenith X1 helmet, developed by a former Harvard University quarterback, claims to have achieved an average severity index score of 340 during certification testing but has not yet been studied in the field.¹⁰)

Without an effective means of preventing concussion, clinicians have instead focused on preventing recurrent concussions from occurring while the brain is still recovering from an initial concussion, known as “second impact syndrome.”¹¹

“If you have a concussion injury and you don't have a secondary insult, in almost all cases within seven days the cells will recover,” Cantu said. “When there is cell death, it's usually due to a secondary insult before the first injury has resolved.”

The clinical challenge, then, is to determine when an athlete who has suffered a concussion has fully recovered to the point where he or she will not risk a secondary injury upon returning to the field. Whereas early guidelines on concussion management tended to associate injury severity with loss of consciousness, many experts now believe that duration of symptoms is a more reliable indicator of injury severity. A 2004 consensus statement recommended that athletes not be allowed to return to play until they are symptom-free both during rest and during exertion.¹² Cantu's revised guidelines, published in 2001,¹³ recommended that athletes with mild (no LOC; post-traumatic amnesia or symptoms lasting less than 30 minutes) or moderate (LOC less than 1 minute, PTA or symptoms between 30 minutes and 24 hours) first-episode concussions be asymptomatic for one week and those with severe concussions (LOC of more than 1 minute or PTA for more than 24 hours; symptoms lasting longer than 7 days) wait at least 1 month before returning to play, and only then if they have been asymptomatic for 1 week. (Cantu's guidelines are stricter for second and third episodes, recommending termination of the season following a second severe concussion or a third mild or moderate concussion.)

TESTING WELL

Some symptoms, such as loss of consciousness or loss of balance, will be obvious to clinicians and athletes alike. But others, such as headache, light-headedness, fatigue, or impaired vision, may be easier for athletes to hide from coaches, trainers, or physicians if they are anxious to return to action. That's where neurocognitive and neuropsychological tests—some of which have been computerized to minimize the manpower needed for administration—can play an important role.^14-18 If clinicians obtain baseline testing data on athletes before the start of a sports season, then those baseline scores can serve as normative comparisons to scores achieved following a concussion.

Some are concerned, however, that clinicians may become overly reliant on testing.

“Remember that neuropsychological testing is only one tool in the toolbox,” said Margot Putukian, MD, director of athletic medicine and head team physician for Princeton University. “We have to ask ourselves, if we use neuropsychological tests, are we forgetting about our clinical skills?”

As an example, Kelly recalled how former National Hockey League star Pat Lafontaine, while recovering from a concussion during his playing career, scored extremely well on a neuropsychological test but after finishing the test grabbed the back of his chair and confessed that he felt as if he were about to pass out.

“Neuropsychological testing is sometimes used as the only measure to return, and that's just not appropriate,” said Kelly, who added that he and his colleagues often require a normal gradient echo magnetic resonance imaging scan for return to play in addition to normal test scores and absence of symptoms. “There's no reason in this setting to do neuropsychological testing if the patient is still symptomatic. If they're still symptomatic, even if they nail the neuropsych test, we're not going to let them return to play.”

It's also important for clinicians to realize that not all concussions are created equal, and researchers have yet to identify accurate predictors of concussion risk or recovery times. The Head Impact Telemetry System (HITS), developed by Simbex, has allowed University of North Carolina researchers to track accelerations and impacts for each play made by a football player wearing an instrumented helmet, but early results presented in June at the American College of Sports Medicine meeting suggested no significant relationship between impact magnitude or location and acute clinical symptoms, according to Kevin Guskiewicz, PhD, ATC, chair of exercise and sport science at the university and lead author of the UNC survey studies on recurrent concussion in former NFL players.

“You can't just look at a particular hit on the field and say, there's a concussion,” Lovell said. “We see these horrendous collision sometimes that for some reason don't result in a concussion. On the other hand, on any given Sunday—or Saturday, or Friday night—you'll see a collision that looks to be quite minimal and yet the athlete will have concussion symptoms. There are no set rules.”

GENDER INEQUALITY

One factor that may affect the impact of concussion is gender, something that has only very recently become part of the concussion discussion.^19,20 In a study of 2340 male and female high school and college athletes,¹⁹ researchers from the University of Virginia found that female athletes who suffered concussions experienced greater declines in reaction time relative to baseline levels, more post-concussion symptoms, and 1.7 times greater level of cognitive impairment than their male counterparts.

The reasons for this discrepancy are as yet unknown but are likely complex, said lead author Donna K. Broshek, PhD, associate professor of psychology and neurobehavioral sciences and associate director of the brain injury and sports concussion institute at the university. Possibilities include hormonal effects on risk of neurological injury, biomechanical differences between men and women, or the failure of certain sports to acknowledge the aggressiveness of female athletes.

“Lacrosse is a perfect example,” Broshek said. “Male players wear large impressive helmets and females wear an eye mask. That's because in the women's game are that you're not supposed to hit above the waist with the stick. Well, sometimes rules don't get followed.”

Regardless of why the gender-based differences occur, the findings underscore the importance of basing return to play guidelines—for either gender—on an individual athlete's performance relative to his or her baseline levels, Broshek said..

“We need to protect athletes on an individual basis,” she said. “If you have a brain injury, it changes everything about you in a matter of seconds. You can have a concussion and absolutely return safely to play, but we need to make sure you are completely recovered before you go back in.”

References

1.Jordan BD, Relkin NR, Ravdin LD, et al. Alipoprotein E4 associated with traumatic injury in boxing. JAMA 1997;278(2):136-140.

2.Schwarz A. Dark days follow hard-hitting career in N.F.L. New York Times. February 2, 2007.

3.Zetterberg H, Hietala MA, Jonsson M, et al. Neurochemical aftermath of amateur boxing. Arch Neurol 2006;63(9):1277-1280.

4.Omalu BI, DeKosky ST, Minster RL, et al. Chronic traumatic encephalopathy in a National Football League player. Neurosurgery 2005;57(1):128-134.

5.Omalu BI, DeKosky ST, Hamilton RL, et al. Chronic traumatic encephalopathy in a national football league player: part II. Neurosurgery 2006;59(5):1086-1092.

6.Guskiewicz KM, Marshall SW, Bailes J, et al. Recurrent concussion and risk of depression in retired professional football players. Med Sci Sports Exerc 2007;39(6):903-909.

7.Guskiewicz KM, Marshall SW, Bailes J, et al. Association between recurrent concussion and late-life cognitive impairment in retired professional football players. Neurosurgery 2005;57(4):719-726.

8.Swartz J. Doctor: Wrestler Benoit had 'shocking' brain damage. USA Today. September 5, 2007.

9.Pellman EJ, Viano DC, Tucker AM, et al. Concussion in professional football: Location and direction of helmet impacts—Part 2. Neurosurgery 2003;53(6):1328-1341.

10.Schwarz A. Helmet design absorbs shock in a new way. New York Times. October 27, 2007.

11.Saunders RL, Harbaugh RE. The second impact in catastrophic contact-sports head trauma. JAMA 1984;252(4):538-539.

12.McCrory P, Johnston K, Meeuwisse W, et al. Summary and agreement statement of the 2nd International Conference on Concussion in Sport, Prague 2004. Br J Sports Med 2005;39(4):196-204.

13.Cantu RC. Posttraumatic retrograde and anterograde amnesia: Pathophysiology and implications in grading and safe return to play. J Athl Train 2001;36(3):244-248.

14.Van Kampen DA, Lovell MR, Pardini JE, et al. The “value added” of neurocognitive testing after sports-related concussion. Am J Sports Med 2006;34(10):1630-1635.

15.Broglio SP, Macciocchi SN, Ferrara MS. Sensitivity of the concussion assessment battery. Neurosurgery 2007;60(6):1050-1057.

16.Brooks DA. Use of computer based testing of youth hockey players with concussions. NeuroRehabilitation 2007;22(3):169-179.

17.Collins MW, Iverson GL, Lovell MR, et al. On-field predictors of neuropsychological and symptom deficit following sports-related concussion. Clin J Sport Med 2003;13(4):222-229.

18.Echemendia RJ, Julian LJ. Mild traumatic brain injury in sports: neuropsychology's contribution to a developing field. Neuropsychol Rev 2001;11(2):69-88.

19.Broshek DK, Kaushik T, Freeman JR, et al. Sex differences in outcome following sports-related concussion. J Neurosurg 2005;102(5):856-863.

20.Covassin T, Schatz P, Swanik CB. Sex differences in neuropsychological function and post-concussion symptoms of concussed collegiate athletes. Neurosurgery 2007;61(2):345-350.