Spiking Fatigue

Research reveals complexity of athletes' response to fatigue

Published in the April 2008 issue of BioMechanics

by Jordana Bieze Foster


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One of the biggest challenges faced by researchers in search of a link between fatigue and injury risk in athletes is that they don't yet know exactly what they're looking for. Since a study protocol that would fatigue athletes to the point of injury would have little chance of being approved by any Institutional Review Board, investigators have been left with their own best educated guesses as to which protocols best approximate a real-world scenario and which specific variables are most likely to be affected by fatigue in ways that will translate to injury. And as one might expect, the results to date have yielded as many questions as answers.

A spate of recently published papers on fatigue exemplify this. To be sure, these studies demonstrate that fatigue does in fact have an adverse effect on landing mechanics, postural control, and neuromuscular function at the ankle. But they also raise questions as to the relative importance of peripheral fatigue versus central fatigue, whether an athlete's skill level determines fatigue's impact, and why carry-over effects of fatigue are seen in muscles other than those that have been targeted.

“Fatigue's a tough nut to crack,” said Thomas W. Kernozek, PhD, a professor in the department of health professions at the University of Wisconsin-La Crosse.

Impact on impact

Nowhere else in the biomechanics mainstream is the study of fatigue more in vogue at the moment than among those studying landing mechanics in search of risk factors for anterior cruciate ligament injuries, particularly in women (see “Research drives ACL injury investigation,” September 2006, page 22). The most recent contribution to that discussion came from Kernozek and colleagues, in a paper published in the March issue of the American Journal of Sports Medicine1 that compared the effects of neuromuscular fatigue on landing mechanics in male and female athletes.

In the La Crosse study, 14 female and 16 male recreational athletes performed single-leg drop landings from a height of 50 cm before and after completing a fatigue protocol in which they performed parallel squats, with weights set at 60% of their one-repetition maximum level, until they could no longer lift the weight.

Following the fatiguing exercise, both men and women tended to land with greater hip flexion and ankle dorsiflexion, along with lower knee extension and abduction moments. This latter finding is in contrast to that of a similar study from the Cleveland Clinic and the University of Michigan,2 published in March 2007, which found that fatigue not only increased the knee abduction moment but did so to a greater extent in women than in men.

The two sets of findings also differed with regard to the effect of fatigue on sagittal plane motion and tibial shear force. The La Crosse study found that, in the presence of fatigue, peak knee flexion on landing increased significantly in male athletes but did not change in female athletes. In addition, the female study subjects demonstrated significantly greater degrees of anterior tibial shear force when fatigued, whereas shear force in the male subjects did not change significantly. The 2007 study, on the other hand, found no gender-related differences in the effects of fatigue on either peak knee flexion or posterior tibial shear force.

The relative contribution of sagittal plane mechanics to ACL injury risk is a subject of some debate within the biomechanics community, with the authors of the 2007 fatigue study maintaining that frontal plane mechanics likely play a greater role (see “Clash over knee flexion reflects complexity of ACL risk research,” September 2005, page 11). The findings from the La Crosse team seem to fall into the opposing camp, suggesting that by landing in a more flexed position, fatigued male athletes are able to protect the knee joint from potentially injurious shear forces.

“Both things point toward females not being able to respond as well with fatigue,” Kernozek said.

Delving into differences

It's also possible, however, that the discrepancies between the two sets of findings reflect differences in study population and study design that may also prove to be clinically important.

Whereas the La Crosse study involved recreational athletes, the subjects in the 2007 study played basketball, soccer, or volleyball for NCAA division I teams. Kernozek and Scott G. McLean, PhD, who helmed the 2007 study while at the Cleveland Clinic but has since become director of the Injury Biomechanics Laboratory at the University of Michigan, both suggested this could in part explain the divergent findings.

“Athletes that jump and land for a living may have more ability to adapt to fatigue than a recreational athlete,” McLean said. “I'm testing recreational athletes now, because in a university setting it's what's available, and we definitely see that responses to fatigue are very different in this group. They tend to be more random, and we don't see that ability to adapt.”

Then there's the issue of the fatigue protocol. In the 2007 study, subjects performed four minutes of continuous drills that included rapid step up/down movements and plyometric bounding movements. Because that protocol was intended to simulate an actual athletic competition, it likely had a more central fatigue effect than that of the La Crosse study, McLean said. In fact, McLean said his group's subsequent fatigue study3 incorporated a protocol that was more like the La Crosse squatting regimen in order to more effectively fatigue the specific muscles involved in landing.

However, McLean's more recent study, published in the January issue of Clinical Biomechanics, suggests that even a more specific fatigue protocol has effects beyond that of the targeted muscles. In analyzing 25 female NCAA athletes, McLean and colleagues found that the effects of fatigue on single leg drop landing mechanics were even more pronounced when the landings were unanticipated—suggesting that fatigue impairs decision-making as well as muscle function.

“I'm pretty convinced that there's a component of this occurring at supraspinal level,” McLean said. “Either they make poor decisions, or they make the right decision but it takes longer to process.”

Protocol roulette

Further complicating the fatigue-protocol puzzle are findings from the University of Idaho, published in February in the online version of the Scandinavian Journal of Medicine & Science in Sports.4 Although the Idaho researchers examined postural control rather than landing mechanics, and involved healthy college-age volunteers rather than athletes, their surprising finding that global fatigue and targeted muscular fatigue had similar effects may have implications for researchers in other realms.

“It's a red flag, suggesting that it doesn't really matter what type of fatigue an individual is getting, it's still going to affect their postural control,”said D. Clark Dickin, PhD, an assistant professor in the department of health, physical education, recreation and dance at the university.

The Idaho investigators used a Neurocom Smart Balance Master system to measure postural sway during unilateral stance in the 16 volunteers before and within 20 seconds after one of three fatigue protocols, as well as 10, 20 and 30 minutes post-fatigue. One fatigue protocol involved isokinetic contractions of the flexors and extensors of the ankle on a Cybex dynamometer until the subject was unable to perform three consecutive contractions at or above 70% of maximum effort. A second protocol was identical, except that the isokinetic contractions were performed at the knee rather than the ankle. The third protocol involved continuous bilateral squat jumps to the point where the subject could not reach 80% of maximum jump height on three consecutive jumps. At least 48 hours elapsed between each fatigue regimen.

All subjects demonstrated significantly greater postural sway in the antero-posterior direction immediately post-fatigue, at 10 minutes and at 30 minutes (values at 20 minutes were not statistically significant but trended toward significance). However, the fatigue effect did not differ significantly between fatigue protocols at any time point.

“That it resulted in the same rate of change was a surprise to me,” Dickin said. “The jumping protocol was a lot faster than what we were doing with the Cybex, and a lot of the subjects were out of breath. That's why I expected to see more of an effect after the 30 minutes of rest.”

When the balance platform was sway-referenced to test subjects' postural control in an altered somatosensory environment, the researchers found that sway increased significantly. However, they also found that sway-referenced postural control was not affected by any of the fatigue protocols.

“We did find an increase in postural sway by taking away sensory information. That was no surprise,” Dickin said. “Fatigue doesn't exacerbate that in any way, as far as we've found.”

Although Dickin and colleagues do not typically work with athletes and are more interested in applying their findings to the elderly population, he suggested that a similar study might yield different results in a more active study population.

“An athlete is probably going to be more resistant to fatigue, and recover faster. In terms of how that impacts their postural control, I would hazard a guess that they might recover faster, but I don't know, he said. “That's where the altered somatosensory conditions may tease something out.”

Sub-prime risks

Just as several different fatigue protocols may have similar effects, a November study5 from the University of Delaware suggests that a single fatigue protocol may affect muscles other than those that have been specifically targeted.

The Delaware researchers assessed the neuromuscular function of the ankle musculature in 16 college-aged volunteers, before and after a fatigue protocol in which the subjects performed continuous concentric and eccentric movements on a KinCom isokinetic dynamometer at 120º/sec until peak torque decreased to 50% of maximum levels for three consecutive eccentric movements. Subjects were tested on inversion/eversion movements in one session and plantar flexion/dorsiflexion movements in a second session, in random order, with at least 72 hours separating the two sessions.

Overall, fatigue was associated with decreases in force production, peak activation and median frequency of the muscles considered to be the prime movers for each motion. However, plantar flexion fatigue also had the effect of decreasing activation and median frequency in the peroneal muscles, which are primarily lateral stabilizers and have only a secondary role in plantar flexion. This suggests that fatigue associated with plantar flexion movements—including jumping and landing—may in turn increase the risk of an inversion ankle sprain.

“You have to keep in mind the whole system when you're trying to theorize about the effects of fatigue on injury risk,” said Greg M. Gutierrez, a doctoral student and research assistant in the Human Performance Laboratory at the university and first author of the study. “Just because you're doing a movement that is primarily plantar flexion, that doesn't mean that these other muscles aren't being fatigued.”

Although the Delaware researchers did observe greater inversion torque with fatigue in male subjects than in female subjects, after normalization for body weight differences, but Gutierrez said this was more likely a gender-related difference in adaptation to the test itself rather than an indication of gender differences in injury risk. Although a 2000 study in Clinical Orthopaedics and Related Research6 reported a 25% greater risk of ankle injury in female basketball players than their male counterparts, a number of other epidemiological studies7-10 have failed to document any gender bias for ankle sprain.

And although the Delaware study subjects were not elite athletes, Gutierrez speculated that elevating the skill level of the test subjects would not change the nature of the findings.

“With elite level athletes, the only difference I would expect to find is that it would take them longer to reach fatigue,” he said. “I would imagine that the final results would be very similar, if not more statistically significant. They would have had to put so much effort into fatiguing those muscles that it would potentially have had more of an effect.”

Injury implications

With research continuing to demonstrate the effects of fatigue, two significant questions remain. One, of course, is which of these effects—if any—actually contribute to injury risk.

“That's essentially the problem with fatigue research,” Gutierrez said. “We can come up with all these variables that we think would suggest would increase risk of injury, but nobody to date has really been able to make the tie between fatigue and injury.”

Assuming such a link can be found, the second question is what can be done about it. Injury prevention programs, like the one popularized by Cincinnati Children's Hospital,11 may benefit from incorporating some endurance elements to better approximate the effects of fatigue that will inevitably be part of a game situation.

“Some sort of interval or circuit type programming should be implemented, where athletes perform bouts of exercises within a set time and are pushed to a state of fatigue. We try to implement that in some of the clinics we work with,” Kernozek said. “Just working on mechanics in isolation, you never get to that state. But they're definitely going to reach that state during a game.”

Jordana Bieze Foster is a freelance medical writer based in Massachusetts and former editor of BioMechanics magazine.

References

1.Kernozek TW, Torry MR, Iwasaki M. Gender differences in lower extremity landing mechanics caused by neuromuscular fatigue. Am J Sports Med 2008;36(3):554-565.

2.McLean SG, Felin RE, Suedekum N, et al. Impact of fatigue on gender-based high-risk landing strategies. Med Sci Sports Exerc. 2007;39(3):502-514.

3.Borotikar BS, Newcomer R, Koppes R, McLean SG. Combined effects of fatigue and decision making on female lower limb landing postures: central and peripheral contributions to ACL injury risk. Clin Biomech 2008;23(1):81-92.

4.Dickin DC, Doan JB. Postural stability in altered and unaltered sensory environments following fatiguing exercise of lower extremity joints. Scand J Med Sci Sports 2008 Feb 2 [Epub ahead of print]

5.Gutierrez GM, Jackson ND, Dorr KA, et al. Effect of fatigue on neuromuscular function at the ankle. J Sport Rehabil 2007;16(4):295-306.

6.Hosea TM, Cary CC, Harrer MF. The gender issue: epidemiology of ankle injuries in athletes who participate in basketball. Clin Orthop Relat Res 2000;372:45-49.

7.Beynnon BD, Murphy DF, Alosa DM. Predictive factors for lateral ankle sprains: a literature review. J Athl Train 2002;37(4):376-380.

8.Deitch JR, Starkey C, Walters SL, et al. Injury risk in professional basketball players: a comparison of Women's National Basketball Association and National Basketball Association athletes. Am J Sports Med 2006;34(7):1077-1083.

9.Zelisko JA, Noble HB, Porter M. A comparison of men's and women's professional basketball injuries. Am J Sports Med 1982(5);10:297-299.

10.Junge A, Langevoort G, Pipe A, et al. Injuries in team sport tournaments during the 2004 Olympic Games. Am J Sports Med. 2006;34(4):565-576.

11.Hewett TE, Lindenfeld TN, Riccobene JV, Noyes FR. The effect of neuromuscular training on the incidence of knee injury in female athletes: a prospective study. Am J Sports Med 1999;27(6):699-706.


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