By Avery Hinks In a previous knowledge translation, we discussed the proverbial “Old Man Strength.” As we age, our muscles become weaker. However, this loss of strength is seen primarily in concentric (shortening) and isometric (static) muscle contractions. In eccentric (lengthening) muscle contractions, strength is well-maintained into old age. An important feature of eccentric contractions is their ability to induce muscle damage. When performing many repeated, high-intensity eccentric contractions, the structures within your muscle called sarcomeres stretch so drastically that they tear apart. As a result, the muscle becomes injured, with deficits in strength lasting as long as a week. Alongside loss of strength, injuries can also be more severe and prevalent in old age. Knowing eccentric strength is maintained in old age, however, you might wonder if older individuals are also protected from further muscle injury induced by eccentric exercise. The short answer is a common phrase in the field of muscle physiology: “it depends.” What do studies on animals show?In the 1990s, there were two prominent investigations into the influence of old age on muscle damage following eccentric exercise. One of these investigations was in mice, and the other in rats. The first study, by Brooks and Faulkner, exposed old (~27 months old) and young (~3 months old) mice to eccentric exercise. They used the ankle dorsiflexor muscle group (the muscles used to point your toes up toward your head), and the exercise consisted of three 5-minute bouts of eccentric contractions. The graph above shows recovery of maximum strength in the young and old mice 3 to 28 days following the eccentric exercise. At 3 days, the old and young mice both exhibited a ~35% drop in strength compared to pre-exercise. These results indicate old and young mice experienced a similar degree of muscle damage. Old and young mice differed in their long-term recovery, however. Young mice recovered over 80% of their initial maximum strength at 14 days and were fully recovered by 28 days. Old mice did not even recover to 80% by 28 days. An additional assessment at 60 days also showed they still had not recovered. In 1995, McBride and Carlsen performed a similar study on old (~32 months old) and young (~6 months old) rats. Their investigation also used the ankle dorsiflexors, and consisted of four sets of six eccentric contractions. In the graphs above, focus on the values at 250 Hz (underlined in red), as those are the indicators of maximum strength. Like the mouse study, the young and old rats exhibited about the same initial drop in maximum strength (about 30% of pre-exercise) at 1 and 2 days following eccentric exercise. When tested at 5 days, the young rat muscles had recovered while the old rats remained deficient in strength by about 18%. This rat study went one step further than the mouse study, though. Another common feature of eccentric exercise is that, in the weeks following the exercise, muscle adapts and is protected from damage in a subsequent bout. This phenomenon is called the “repeated bout effect” and was discussed in detail in a previous knowledge translation. Two weeks after the initial eccentric exercise bout, McBride and Carlsen exposed the rats to a second, identical bout of eccentric exercise. The young rats perfectly demonstrated the repeated bout effect, showing no drop in maximum strength two days post-exercise. The old rats, however, still exhibited a deficit in strength, indicating their muscle did not fully adapt in the 2 weeks between exercise bouts. These rodent studies together have two key takeaways:
But do these results translate to humans? What have studies on humans shown?One of the earliest investigations of susceptibility to damage induced by eccentric exercise in old versus young humans was by Dedrick and Clarkson in 1990. They exposed the forearm flexor muscles of young (~24 years old) and older (~67 years old) women to 24 eccentric contractions. Like the studies on rodents discussed above, young and older women experienced a similar reduction in isometric strength immediately following the eccentric exercise, and older women took longer to recover. The graph below clearly shows a large difference in maximum isometric strength between the young and older women at 5 days. So, there we go! Older humans take longer to recover following eccentric exercise, right? This is where it gets tricky. The next notable studies on this topic were conducted by Lavender and Nosaka in 2006. They subjected the elbow flexor muscles of young (~19 years old) and older (~70 years old) men to six sets of five eccentric contractions. Based on Dedrick and Clarkson’s earlier work, they reasonably expected the effects of eccentric exercise-induced muscle damage to be worse in the older men. They ended up observing the opposite! Not only did the older men experience less of a reduction in strength following the eccentric exercise, they recovered faster over the course of 10 days. This difference is shown in the graph below, with the black circles representing old and the white squares representing young. In a follow-up, study, however, Lavendar and Nosaka confirmed in humans one of the key take-aways from the rodent studies. After a second bout of eccentric exercise performed 4 weeks later, young men adapted such that their strength recovered sooner. Conversely, older men recovered no different than following the first bout. For these studies on humans, we should consider the exercise intensity. In Clarkson and Dedrick’s studies, they used maximal eccentric contractions, whereas Lavender and Nosaka’s eccentric contractions equated to about 40% of maximum strength. Perhaps older individuals are more protected from muscle damage in lower intensity eccentric contractions, but experience blunted recovery as intensity increases. Later studies seem to confirm this speculation. Most notably, Chapman and colleagues employed eccentric contractions of the elbow flexors, like Lavender and Nosaka. This time, the eccentric contractions were performed at a maximal intensity and at a faster speed (faster speeds also increase the intensity of eccentric contractions). As shown in the graph below, older men had a severely delayed recovery of strength compared to young men. But these results may still very, even with maximal contractions. In the ankle dorsiflexors, Skarabot and colleagues found that older adults had faster recovery following an initial eccentric exercise bout—but it doesn’t stop there! Older adults also adapted better following the first bout such that their strength recovered even sooner following a second bout. There may be an explanation for Skarabot and colleagues’ conflicting findings, which I will discuss in a moment. For now, even with the conflicting findings among human studies, we can be confident about two points:
Can we mitigate the greater susceptibility to muscle damage in old age?Researchers have offered several explanations regarding the delayed recovery of older compared to young adults. With old age, the molecular processes behind the muscle’s regenerative capacity decline. As a result, adaptations to unaccustomed exercise can take longer, or not occur at all. Muscles also become shorter as they lose mass with age. When performing eccentric contractions, greater damage occurs the further a muscle stretches. Shorter muscles, then, end up stretching further for a given movement, incurring more damage. This greater damage could contribute to the longer recovery time. Unsurprisingly, physical activity helps to mitigate the development of weakness following eccentric exercise in old age. Ploutz-Snyder and colleagues subjected the knee extensor muscles of young (~23 years old) and older (~66 years old) women to near-maximal eccentric exercise. The older woman were tested both before and after completing a 12-week resistance training program. When untrained, the older women exhibited a 24% loss of strength following eccentric exercise, compared to only 6% in young women. After resistance training, the older women experienced only a 14% loss of strength following eccentric exercise, recovered sooner, and were statistically no different from the young women. Physical activity may also explain the conflicting findings presented by Skarabot and colleagues above (the graph is shown again below for your convenience). The older adults enrolled in that study reported partaking in on average 330 minutes of moderate to high-intensity physical activity per week. Maybe that particular sample of older adults didn’t exhibit an inability to recover or adapt following eccentric exercise because of their active lifestyles. ConclusionSo, does the maintenance of eccentric strength in old age protect older individuals from further exercise-induced muscle damage? Older individuals seem to experience no further weakness following high-intensity eccentric exercise than young individuals, and may even experience less weakness than young if the eccentric exercise is moderate-intensity. Where they differ is in the recovery and the ability to adapt following the exercise, with old showing clear impairments. The good news is these impairments can be mitigated by physical activity—even if physical activity is started when already in old age! What we’re less certain about is what specifically is going on within the muscle’s structure to drive these differences between young and older adults. Our lab is currently looking into this in groups of old and young rats, so that discussion will have to wait for another day.
References Brooks, S. V., & Faulkner, J. A. (1990). Contraction-induced injury: recovery of skeletal muscles in young and old mice. American Journal of Physiology-Cell Physiology, 258(3), C436–C442. doi:10.1152/ajpcell.1990.258.3.C436 Chapman, D. W., Newton, M., McGuigan, M. R., & Nosaka, K. (2008). Comparison between old and young men for responses to fast velocity maximal lengthening contractions of the elbow flexors. European Journal of Applied Physiology, 104(3), 531–539. doi:10.1007/s00421-008-0806-7 Clarkson PM, Tremblay I. Exercise-induced muscle damage, repair, and adaptation in humans. J Appl Physiol (1985). 1988 Jul;65(1):1-6. doi: 10.1152/jappl.1988.65.1.1. PMID: 3403453. Dedrick, M. E., & Clarkson, P. M. (1990). The effects of eccentric exercise on motor performance in young and older women. European Journal of Applied Physiology and Occupational Physiology, 60(3), 183–186. doi:10.1007/bf00839156 Lavender, A. P., & Nosaka, K. (2006). Comparison between old and young men for changes in makers of muscle damage following voluntary eccentric exercise of the elbow flexors. Applied Physiology, Nutrition, and Metabolism, 31(3), 218–225. doi:10.1139/h05-028 Lavender, A. P., & Nosaka, K. (2006). Responses of old men to repeated bouts of eccentric exercise of the elbow flexors in comparison with young men. European Journal of Applied Physiology, 97(5), 619–626. doi:10.1007/s00421-006-0224-7 McBride, T. A., Gorin, F. A., & Carlsen, R. C. (1995). Prolonged recovery and reduced adaptation in aged rat muscle following eccentric exercise. Mechanisms of Ageing and Development, 83(3), 185–200. doi:10.1016/0047-6374(95)01629-e Ploutz-Snyder, L. L., Giamis, E. L., Formikell, M., & Rosenbaum, A. E. (2001). Resistance Training Reduces Susceptibility to Eccentric Exercise-Induced Muscle Dysfunction in Older Women. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, 56(9), B384–B390. doi:10.1093/gerona/56.9.b384 Škarabot, J., Ansdell, P., Temesi, J., Howatson, G., Goodall, S., & Durbaba, R. (2019). Neurophysiological responses and adaptation following repeated bouts of maximal lengthening contractions in young and older adults. Journal of Applied Physiology. doi:10.1152/japplphysiol.00494.2019
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