Research links concussion, ACL injury, and gender: A roundtable discussion

Physicians who make a habit of attending the annual meeting of the American Orthopedic Society for Sports Medicine are accustomed to seeing scientific presentations on gender and injury risk. The increased risk of anterior cruciate ligament injuries in female athletes, in particular, has been a topic of discussion at AOSSM meetings since 1996.

But this past summer, the AOSSM program featured a scientific presentation on a possible link between gender and a different type of injury: concussion, which University of Pittsburgh researchers linked to more serious symptoms in female soccer players than their male counterparts.¹

At first glance, the topic might seem out of place at a meeting of physicians who focus on bones and joints. But for the many orthopedists who serve as team physicians, diagnosing and managing concussion is becoming more and more a part of their job description.

And as a growing number of studies^1-7 suggest that gender may play a role in concussion risk, some intriguing parallels have become apparent between this emerging field of study and that of gender and ACL injury. Some researchers are even starting to wonder if these two apparently disparate types of injuries may actually have other risk factors in common—risk factors that might prove key to effective prevention.

BioMechanics brought together a panel of experts on gender and either ACL injury or concussion to explore these issues and what they might mean for athletes and the practitioners who care for them.

Focus on biomechanics

From the beginning, the study of gender and ACL injury has focused on biomechanics. Researchers have found that certain aspects of the techniques athletes use in landing from a jump or changing direction are associated with increased risk of ACL injury, and more so in female athletes than in male athletes.^8-11 They've also demonstrated that neuromuscular training programs designed to correct these high-risk mechanics can help reduce injury rates.^12-14

But not all training programs have led to reductions in injury rates,^15-16 and even those that have been effective have not eliminated risk.^17-18 Though compliance may well be an issue, researchers keep coming back to the idea that there may be more to the ACL injury mechanism than is currently understood.

University of Michigan investigators and others have suggested that neural control may play an important role, although the level at which that neural control occurs and the extent to which neural control differs between genders are open questions at this point.^19-21

Concussion defies definition

In the study of concussion, much of the focus has been on simply defining the injury. Unlike an ACL tear, concussion cannot be verified using imaging or surgery, so accurate identification of concussion symptoms (Tables 1 and 2) is essential for patient management.^22-23 Concussed athletes who return to play before all symptoms have resolved run the risk of further injury or “second impact syndrome,”²⁴ which is thought to have been responsible for the October death of a high school football player in New Jersey.

The biomechanics of concussion are similarly complicated, taking into account both the way the head is struck and the way it responds to the impact.^25-27 Studies utilizing motion analysis and instrumented football helmets have found that rotational forces, resulting from impacts to the forehead or side of the head, are those most likely to be associated with concussion symptoms. Newer models of football helmets designed to better withstand these impacts have been shown to decrease concussion incidence significantly but still do not come close to eliminating the risk.²⁸

Researchers have theorized that neck muscle strength also can be protective against these impacts, and that female athletes' increased risk may be related to smaller and weaker neck muscles than those of male athletes. However, early research also suggests that strengthening alone does not improve an athlete's ability to withstand a blow to the head,²⁹ just as strengthening alone does not seem to be enough to improve landing mechanics in athletes at risk for ACL injury.³⁰ This suggests that neural control of muscle function may play an important role in the mechanism of concussion as well as ACL injury.

Neurological and behavioral factors

Certainly many of the symptoms associated with concussion are neurological and behavioral as well as physical. For this reason, computerized neuro-psychological tests such as ImPACT (Immediate Post-Concussion and Cognitive Testing) have been utilized to assess symptoms that may not be readily apparent to a coach or trainer.^31-35 A preseason test establishes baseline scores for each athlete; following a concussion, guidelines suggest that athletes not return to play until those scores return to baseline levels and there is a complete resolution of physical symptoms.

These neuro-cognitive factors would appear to be unique to concussion. But a June 2007 retrospective study³⁶ from the University of Delaware found that baseline ImPACT scores for collegiate athletes who went on to sustain ACL injuries were significantly different from scores for uninjured athletes.

It may be a leap of faith to conclude that neuro-cognitive function is predictive of either ACL injury or concussion, and if so, it remains unclear how or even if gender might factor into the equation. But the possibilities certainly are interesting.

Panelists

Kevin M. Guskiewicz, PhD, is chair of the department of exercise and sport science and a professor of orthopaedic surgery at the University of North Carolina. His group has published extensively on concussion epidemiology, risk factors and outcomes, and has made headlines recently for research linking concussion history to cognitive impairment and depression in former professional football players.

Timothy E. Hewett, PhD, is director of the Sports Medicine Biodynamics Center at Cincinnati Children's Hospital, an assistant professor of pediatrics and orthopedic surgery and an adjunct associate professor of rehabilitation sciences at the University of Cincinnati. His group has been at the forefront of research on gender and ACL injury, identifying biomechanical variables that are predictive of injury and developing a neuromuscular training program.

Margot Putukian, MD, is director of athletic medicine and head team physician at Princeton University and associate clinical professor of family practice at the University of Medicine and Dentistry of New Jersey. She has provided a real-world perspective on concussion as a participant in multiple international consensus conferences and a speaker at clinical society meetings.

Mark R. Lovell, PhD, is founding director of the Sports Medicine Concussion Program and an associate professor of orthopaedic surgery and neurological surgery at the University of Pittsburgh. He founded the neuropsychological testing program for the National Football League and is the former director of the National Hockey League's neuropsychology program. He also developed the ImPACT test, in partnership with Joseph Maroon, MD.

Note: Dr. Lovell's comments were included following his review of the comments made by Drs. Guskiewicz, Hewett, and Putukian.

BioMechanics: It seems that in many ways concussion research is at a point where ACL injury research was maybe 10 years ago. There are studies that suggest a difference between genders in terms of concussion incidence, and there has been some discussion of the risk factors that might be involved. But not a lot is going on yet with regard to interventions, and there is still a lot of work to do in terms of completely understanding the concussion injury mechanism and what, if anything, it has to do with gender.

Putukian: When you’re dealing with concussion, it’s very different than having a physical exam and then an MRI or an arthroscopy to confirm that you have an ACL tear. With concussion, the hard part is defining the injury. The hallmark of concussion is confusion.

If someone has a head blow and then develops a headache and some dizziness, that can be considered a concussion. At the same time, headache is the most common symptom reported by anybody going to the ER, and it can be caused by myriad conditions. I’ve had two kids this fall that we disqualified from playing football--one because of persistent concussive symptoms and one for numerous unreported concussions. And you always wonder if you’re being too conservative or if you’re missing something because they may have headaches for other reasons.

Guskiewicz: Concussion is a hidden epidemic. We can’t see it; it’s not as obvious. If a football player has a dislocated ankle, we know that he’s not going back today, we know he’s not going back tomorrow, next week, next month and his career could be over. With concussion, the injury is just as serious, maybe more serious, but in many cases we don’t know the answer to any of those questions.

Lovell: I agree that concussion is a very difficult injury to deal with because we don't have all the answers. In the final analysis, we may be too conservative, but we probably should be at this time. Headache may or may not be a pernicious symptom. All second impact syndrome cases that I know of had a headache that was not reported or hidden. The recent death in New Jersey is just one of many examples. We are working with fMRI studies to parse this out.

Putukian: I think concussion in general is an under-reported injury. So when you look at some of the studies have shown that this is a more common injury in girls than boys or in college women compared to college men, one thing that comes to my mind is that women are maybe more likely to report their symptoms. If we had 100% reporting, that might affect some of those apparent gender differences.

Guskiewicz: I’ll be honest with you, I sit on the side of this fence with respect to concussion that believes there’s not a gender difference. I think there are other factors that we really haven’t addressed in an appropriate way, such as just behavioral differences between men and women in reporting injuries. We need to do that before we jump on this gender train that suggests that women are more at risk for concussion than men, because I’m not convinced that they are. If you really look at the data closely, only two sports--basketball and hockey--appear to show that this difference may exist, where female players tend to show a slightly higher incidence.

Lovell: I also agree that concussion is underreported. We really have no idea about prevalence. The fact that we see 150 concussed kids per week in Pittsburgh gives us an indication that it is a frequent occurrence.

I agree with Kevin that we have much to learn about gender differences. I would add that injuries do appear to be more prevalent among female soccer players than among males. We have a large study under review that has found significant differences, even when correcting for baseline performance.

Hewett: So there are three different questions here when we’re talking about sex disparity and concussion. The first, is there a difference in incidence? The second, is there a difference in severity? And the third, is there a difference in recovery? John Divine in our group did a study using ImPACT software, and he basically found that the girls rated the severity of their concussion higher than the boys did, and the symptoms took longer to resolve.

Guskiewicz: Even looking at baseline data in normal healthy people, looking at sex differences, we need to remember with respect to concussion that neuro-psych testing is only one piece of the puzzle. We find that men tend to score better on some domains, such as reaction time and math processing, and women tend to do better with verbal recall and some of the memory tasks. So when some studies have found women to recover a little bit differently or maybe more slowly, it may have to do with just reaction time testing where we know there are some clear differences at baseline.

Lovell: One major point about gender issues is that physiological factors may be involved. For instance, any headache specialist will tell you that females have a higher base rate of headaches than males: three to one. Therefore, as a group they may have a higher "loading" to develop headaches post-injury. We also are finding that a family history of headaches makes it more likely that the concussed child will develop headaches post-injury. Does this history also predispose them to concussion? We don't know, but it may be the case.

Putukian: A couple of studies have looked at differences in terms of neuro-psych where women seem to have differences in verbal memory, while men seem to have visual memory issues. And then there's the whole area of how well they resolve or return to their baseline. The whole area of neuro-psych is still very exciting, but I agree it's only one piece of the puzzle.

We’re still learning a lot about the role of neuro-psych testing in concussion. For example, when you do see a difference, when was the baseline test, when was the repeat test done, and what’s the reliable change index for that particular task? Are we sure we know the difference when that kid has taken the baseline test a month before versus taking it a year before?

Hewett: There are potential differences in neuro-psych testing, at least it’s been reported, between the sexes. Then Buz Swanik published that paper that I found quite interesting, in which neuro-psych differences predicted ACL injuries. I think that’s the potential connection of the head bone to the knee bone, as it were. It’s quite intriguing. I don’t know what it means, and if you read Swanik et al's discussion, I don’t think they pretend to know what it means either, but it is interesting.

BioMechanics: Although that study didn’t look at gender specifically.

Hewett: Right, but here’s a question. Prior injury, mainly lower extremity injury, is a really good predictor of future ACL injury. It’s one of the best predictors of future injuries. The question is, if Swanik's data is accurate, would prior concussion, which could potentially alter neuro-psych test scores, increase your risk of future ACL injury?

Putukian: Or any type of injury.

Hewett: Or any type of injury, correct. I think my guess would be there might be a correlation there, but it hasn’t been done. Again, I’m just looking for connections.

Putukian: But a connection based on what?

Hewett: We think neuromuscular control has a lot to do with ACL injury risk and most of the work has been done in women. The question is, if it’s neuromuscular in nature, how much is it neural? And if it’s neural, at what level is it? Is it at the spinal level, is it sub-cortical? Could it be cortical? That’s where a lot of this is going. I’ve just been very skeptical, so far, about the idea that decision making processes could have an effect on an ACL injury risk, given how quickly that injury occurs.

Putukian: One of the mechanisms of ACL injury is deceleration involving a last minute change in direction, such as when a defender has to change direction do to deceive his or her opponent. So it seems that if an athlete’s reaction time or processing speed is diminished, that might put the athlete at risk.

Hewett: With an ACL injury, the time from when that foot hits the ground to when the ligament tears is probably in the range of 50 to 70 milliseconds. Even with spinal level responses, you’re talking about in the range of 80 to 150 milliseconds. So I’ve always thought the effect of neuromuscular training can’t be reactive, it has to be preparatory. How can conscious thought be involved in preventing an ACL injury from a preparatory perspective? You don’t have time to think about that.

BioMechanics: Is there a way to train neural control?

Hewett: You can alter neural control. The thing about it is we don’t know at what level what we do alters it. We’re doing some pretty interesting studies, but most of the studies are too involved to do prospectively in uninjured people. I’m actually writing a grant now trying to convince the NIH that we could do it that way. It’s a bit of a long shot.

Basically we’re looking at the phase shift activity in a task where the person has a biofeedback screen in front of them and there's a square on the screen that moves away from them and then moves towards them. They have their hands crossed over their chest, and they’re balancing on one foot with the other knee at 90/90 and they’re swaying back and forth to keep their face basically parallel to this moving object. We have them do that at low speed and then at high speed.

What normal uninjured people do is at low speed they perform that task with very low variability. It’s relatively easy for them to perform. And then as the frequency increases, the amount of variability increases. That’s what you’d expect from a motor control perspective.

Then we look at the people who have had an ACL reconstruction, right at the point when their physician and physical therapist have released them back to sport. They have a pattern where they perform the slow task with high variability, not low variability, and then it basically doesn’t change at high frequency. Either that or the variability trends down a little bit.

Now we’re using this as a tool for potential prediction of future ACL injury risk. We’ve got a small cohort now who have gone on to second injury. And what we've shown is during the slow task, they do that with very high variability--higher than other people who have had ACL reconstruction. And then, when we move to the high frequency sway task, they sort of lock down the lower extremity and limit the degrees of freedom because it’s quite difficult for them, and their variability goes way down. So it’s the opposite pattern of normal people.

The question is, at what level is this occurring? My guess is this is not at the cortical level, it’s sub-cortical or spinal. Do we know whether we could use training to alter this? I think we probably could. My bias is that this is sub-cortical. If that’s the case and we get back to the whole question of concussion, how does concussion affect sub-cortical pathways? I don’t think we have any idea.

Here's another thought. A lot of coaches think that ACL injury risk is skill-related and doesn't happen to the more skilled players. Well, I think most of the data show that that’s wrong.

Putukian: Correct.

Hewett: This neuro-psych testing could help explain it. You could be a great athlete and still score poorly on a neuro-psych test. But making that connection or even setting up a research design to test it is going to be awfully complex.

Lovell: The research of Buz Swanik and Tracy Covassin is fascinating in terms of looking at this issue. I also agree that we do not really know what it means. ACL injury and concussion could be linked by some type of moderator variable, like neuromuscular control, as mentioned by Tim.

BioMechanics: There isn’t a concussion prevention program along the lines of the ACL prevention program that Tim and other people have developed. Is that because people are reluctant to try to develop such a program without actually knowing more about the mechanism of the injury?

Putukian: I think you’re right. Look how long it’s taken us to figure out the ACL, and there’s still a fair amount of controversy in terms of all the factors that play a role in the mechanism of ACL injury.

Guskiewicz: When you’re dealing with ACL injuries, you can do a bit more to change those predispositions and those differences between the two groups, the two genders. With concussion research, I’m not so sure there’s a whole lot we can do about it.

Where the ACL discussion is similar to the concussion discussion involves gender differences in neck strength. I don’t have any numbers to support the theory, but I do believe the neck strength in the cervical muscles in men, on average, tends to be stronger.

These muscles tend to be more dense and tend to be trained more often in a way that might help prevent concussive injuries than what they are in the female athlete. But to me, that's the only theory that might offer a plausible explanation for why we might see females at a higher risk. Even though, as I’ve already said, I don’t think the true incidence is any higher in females.

BioMechanics: Certainly neck strength is something that you can change.

Guskiewicz: Exactly.

BioMechanics: Mansell et al studied flexion and extension strength exercises for the neck. Although in talking to Bob Cantu about this, he feels that rotational strength is really the key factor. Do you agree with that?

Guskiewicz: I do. Concussion is a diffuse injury, and what we know about the biomechanics of concussion is that it’s not typically from a purely linear blow that causes linear acceleration. It’s more rotational or angular acceleration that causes this diffuse disruption, so we need to find a better way to control those. And there are some biomechanical studies that have begun to look at that, but they do not break out gender as a factor. That, to my knowledge, has not been done.

But I do agree that that’s where we need to control it. And if in fact the neck muscles are not as controlling of the head in the female athlete as in the male athlete, if that were to be true, that might be a plausible explanation for why we potentially see a higher incidence of concussion in women than in men.

BioMechanics: Mansell et al did just look at flexion and extension, and they did look at a combined group of both male and female soccer players. But they found that despite increases in isometric strength and endurance, the program that they used did not enhance head/neck segment stabilization during force application. Would you say that something similar should be done specifically with regard to rotational strength?

Guskiewicz: I think if we’re going to try to relate it to concussion, as Dr. Cantu has said, that’s the most common mechanism for the injury. So that would be an important factor.

BioMechanics: ACL researchers have found that strength training in and of itself doesn’t seem to improve high-risk biomechanics. The theory is that you can strengthen the muscles, but they also need to be retrained somehow so that they know when to activate and that the activation is appropriate to be protective. Can you see things happening along those lines in terms of neck strength?

Guskiewicz: That is an excellent question, and I think that there are some similarities between the way that the ACL researchers are looking at this and the way that we need to be looking at it from the concussion side. Again, the types of mechanisms are so important. One of the studies that we are currently working on is with youth hockey players, where we are studying the way a hockey player braces his or her body and, ultimately, his or her head when they’re ill-prepared versus prepared. In other words, taking an impact blindly from the back or the side.

The head is sitting on top of the neck and then neck muscles sitting on top of the torso sort of act like a swivel, like a bobble-head doll, under those conditions. How can those neck muscles activate in that situation to help protect the brain?

One could argue that maybe they just can’t because the body’s ill-prepared for it, as opposed to seeing a player coming directly at you and being able to brace the body. There, the neck muscles have an opportunity to respond and to be activated in an appropriate way to protect the head. And I think there are some similarities there with the ACL work that’s being done in looking at landing patterns and cutting maneuvers and being able to brace the knee in a way.

But we still have a long way to go before we run an EMG study looking at this. We have accelerometers in the helmets of our hockey players, and we’re looking to see whether when the body is ill-prepared to take that blow the impact to the head is actually of higher magnitude than if the player is bracing for impact. Once we answer that--I think I know what the answer’s going to be, but we want to be sure--then we can take it to the next step.

Putukian: With concussion, I think it’s even harder to discern what the mechanisms of injury are because it’s very different from one sport to the next. I mean, if women’s hockey is not a contact sport, why is the incidence of concussion higher in women’s hockey than in men's?

BioMechanics: Well, just because the rules say you can’t check in women's hockey doesn’t mean it doesn't happen.

Putukian: But there’s certainly not the same level of physical head to head contact in women’s hockey that there is in men’s hockey. There’s some, without a doubt, but there’s certainly not the same amount. And I don’t think that it explains the difference in the incidence of concussion.

Guskiewicz: Part of the problem with hockey is that competitive collegiate women's hockey is still relatively new. I think we do need to take a closer look at the rules and how they’re different. One thing we know is that female hockey players are pretty aggressive, and I think that that may be a factor. I think we really need to look at the rules of the game with regard to that type of aggressive behavior.

BioMechanics: Dr. Putukian, without having access to an intervention that will prevent concussion, what options do you have as a team physician to try to minimize the effects?

Putukian: What we try to do on that end of it really starts with education. It sounds kind of corny, but a lot of our athletes don’t realize that they have had a concussion or that it's important.

An athlete this fall told me that pretty much his sophomore and junior year he had probably had his bell rung, in his words, every game. And that he’d have some difficulty with the next play, maybe the next two plays and he’d have a headache the next day and feel as though he couldn’t concentrate, feel as though he couldn’t work and study, but it would generally go away by Monday. But he never brought it to anyone's concern. Then this particular fall, he’d had a lot of symptoms with what we would consider minor blows. So part of it, I think, is education, just making sure that athletes understand why these are important injuries and why they should report their symptoms.

Then we should certainly try to make sure that they have appropriate equipment. I mean, there’s not much that you can do. The helmets are not designed to prevent concussion, but they should fit appropriately.

Probably the most important issue, and it’s hard to address, is enforcement of rules. The NCAA this year with college football has been trying to do a better job of making sure that head-to-head hits are penalized and that coaches are discouraging kids from using their heads. In soccer, a lot of the head injuries that occur are, again, due to foul play. So you wonder if the rules were enforced better, whether they might be able to prevent some of the injuries.

Then in terms of rehabilitation, once someone’s had a concussion, there’s a delicate balance in terms of activity level. We keep kids out of any activity when they have symptoms, but once their symptoms have resolved, we generally let them back into cardiovascular activity. I think there’s some debate as to at what point do you do more than that, and whether you would do any kind of rehabilitation in terms of the skills you have to use cognitively. Some of our athletes take our hybrid of neuropsychological tests (paper and pencil and the ImPACT test) and the next day complain that they have a headache from taking the test. That may be telling us that they’re not quite ready to proceed. But I think it’s a very interesting area that we need to know more about.

Note: This roundtable was originally published in two parts. References were not included in the published version.

References

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Table 1: Concussion Symptoms

Loss of consciousness (may occur but not required for diagnosis of concussion)

Confusion

Amnesia

Headache

Dizziness

Ringing in the ears

Nausea/vomiting

Slurred speech

Mood and cognitive disturbances

Sensitivity to light/noise

Sleep disturbances

Table 2: American Academy of Neurology Concussion Grading System

Grade 1

Transient confusion

No loss of consciousness

Concussion symptoms or mental status abnormalities on examination resolve in less than 15 minutes

Grade 2

Transient confusion

No loss of consciousness

Concussion symptoms or mental status abnormalities on examination last more than 15 minutes

Grade 3

Any loss of consciousness

Table 3: American Academy of Neurology Return to Play Guidelines

Multiple Grade 1: 1 week

Grade 2: 1 week

Multiple Grade 2: 2 weeks

Grade 3/loss of consciousness < 1 min: 1 week

Grade 3/loss of consciousness > 1 min: 2 weeks

Multiple Grade 3: 1 month or longer