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Point: Skeletal muscle mechanical efficiency does increase with age

2012; American Physiological Society; Volume: 114; Issue: 8 Linguagem: Inglês

10.1152/japplphysiol.01438.2012

8750-7587

Massimo Venturelli, Russell S. Richardson,

Sports Performance and Training

Point:CounterpointSkeletal muscle mechanical efficiency does/does not increase with agePoint: Skeletal muscle mechanical efficiency does increase with ageMassimo Venturelli, and Russell S. RichardsonMassimo VenturelliDepartment of Medicine, Division of Geriatrics, University of Utah, Salt Lake City, Utah (e-mail: ) Department of Neurological, Neuropsychological, Morphological and Movement Sciences, University of Verona, Verona, Italy , andRussell S. RichardsonDepartment of Medicine, Division of Geriatrics, University of Utah, Salt Lake City, Utah (e-mail: ) Geriatric Research, Education and Clinical Center, George E. Whalen VA Medical Center, Salt Lake City, Utah Department of Exercise and Sport Science, University of Utah, Salt Lake City, UtahPublished Online:15 Apr 2013https://doi.org/10.1152/japplphysiol.01438.2012This is the final version - click for previous versionMoreSectionsSupplemental MaterialPDF (45 KB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInWeChat We thank Dr. Ortega for the opportunity to debate the concept that aging affects exercise efficiency. From the outset we must acknowledge that, indeed, some studies report an age-related reduction task efficiency during walking and other rather complex tasks (2, 12, 20, 21). However, in contrast, our recent study of leg cycling in centenarians (28), as well as other work focused more specifically on skeletal muscle function (17, 27), suggests that healthy aging is actually associated with increased mechanical efficiency, likely caused primarily by the age-dependent shift toward an aerobic muscle phenotype (5, 15).Systems energy conservation and efficiency.Important in terms of background, the law of the conservation of energy, first formulated in the nineteenth century, states that total energy in an isolated system remains constant over time. Energy can change its characteristics within the system; for instance, chemical energy can become kinetic energy but that energy can be neither created nor destroyed. Additionally, in terms of energy conversion, the first law of thermodynamics indicates that energy output cannot exceed the input, and the ratio of these two forms of energy describes the efficiency of a system (24): efficiency = output energy/input energy.Muscle energy demand, supply, and efficiency.Although, the well accepted energy-related laws of physics are clearly applicable to isolated systems, human energy supply, demand, and efficiency during exercise, each a consequence of numerous biological systems, are significantly more complex. All the energy required for cellular function, including contractile activity, is provided by the hydrolysis of ATP to ADP and Pi. To balance the significant consumption of ATP during physical activity, efficient pathways of ATP resynthesis are needed. Three main mechanisms facilitate ATP resynthesis in skeletal muscle fibers: creatine kinase activity, glycolysis, and mitochondrial oxidative phosphorylation. Finally, to ensure that all metabolic processes continue to work during sustained exercise, energetic substrates and oxygen must be readily available at the cellular level or supplied via the circulation (23).Previous physiological studies have defined mechanical efficiency as the ratio of the work performed and the amount of oxygen consumed during sustained exercise (8, 22). With this approach, there are convincing data that both in vitro (29) and in vivo (6) the energetic cost of force production is fiber type dependent, with type I or slow-twitch fibers being more efficient than type II or fast-twitch fibers. The mechanisms responsible for the lower cost of developing tension with slow-twitch fibers include higher chemical-to-mechanical coupling efficiency and lower energy cost of the adenosine triphosphatase (ATPase) driven calcium pump whose activity is 5 to 10 times slower in the type I compared with type II fibers (29). The heterogeneity of skeletal muscle metabolic efficiency is also influenced by muscle mitochondrial volume, which varies from ∼6% in type I fibers to ∼4% in type II fibers, and the wide-ranging mitochondrial enzymatic activity in slow- and fast-twitch fibers (14). Thus slow-twitch muscle fibers are designed to generate ATP by oxidative mitochondrial processes, and their relatively low ATP consumption during contraction contributes to their high efficiency. In contrast, fast-twitch muscle fibers that depend more upon glycolytic processes to generate ATP are less efficient during contractile activity (13).Effect of aging on muscle structure, function, and metabolic efficiency.Typically, the percentage of type I fibers is higher in old compared with young muscle, as aging is associated with selective sarcopenia of type II fibers (18, 19). Indeed, this pronounced atrophy of the type II fibers typically results in a greater type I fiber fraction of the total contractile volume in the elderly, which, as already indicated, likely alters metabolic efficiency. Again, due to differences in myosin ATPase and the cost of calcium handling, metabolic efficiency is significantly higher in type I fibers with respect to type II fibers, (7, 9, 25, 26). By using an animal model (10), this concept was translated to reveal increased skeletal muscle metabolic efficiency in senescent rats that had a significant decrease in type II myosin heavy chain content, which was not evident in the middle-aged animals. In humans there are also data that support this phenomenon, with age-dependent changes in fiber-type composition playing a key role in the reduced contractile cost in older men and subsequent increases mechanical efficiency (27).The age-related shift toward a slow-twitch muscle fiber phenotype contributes to an overall slowing of skeletal muscle contractile properties, causing a change in the force frequency relationship (1). Consequently, it is possible that attenuated kinetics may reduce the ATPase rate of type I muscle fibers, contributing to an increase in metabolic efficiency. Thus, the higher relative force at lower stimulation frequencies in older skeletal muscle likely reduces the energy required for ion transport and lessens the motor drive needed to maintain a given relative workload. Indeed, the recent literature indicates that type I myosin kinetics are, indeed, slowed in older humans, primarily driven by modifications of the myosin molecule (11).Certainly, some aspects of muscle performance decline with age; however, recent research indicates that muscular endurance is actually enhanced in older subjects (4, 16). Moreover, it is evident that fiber type differences in healthy long-lived subjects, such as centenarians, may explain the difference in mechanical efficiency observed during exercise (28). It is highly likely that age-related changes in skeletal muscle phenotype can work synergistically with changes in activation pattern, increasing muscle metabolic efficiency in older muscle.Influence of age range and exercise task on mechanical efficiency.Again, it must be recognized that, although an age-related increase in mechanical efficiency has been documented in an animal model (10), in humans, utilizing an MRI approach to interrogate the muscle itself (27), and during cycling exercise in extremely longevous subjects (28), there are certainly other investigations that have failed to reveal this phenomenon (2, 20, 21). However, there are two main differences between these studies that may explain these contrasting results. First, the differing age range of the subjects studied: Bell et al. (2) revealed that in 70-year-old women, net and mechanical efficiency during cycling was significantly reduced. However, recent studies have revealed that the greatest effect of sarcopenia in the locomotor muscles occurs after the 8th decade of life (3). In line with this observation, the older subjects in this study exhibited a maintained percentage of type I fibers and a greater number of type IIx fibers of vastus lateralis compared with young subjects. In contrast, centenarians, an example of extreme human aging, who are likely to exhibit pronounced age-related changes in muscle phenotype, did, in fact, demonstrate enhanced mechanical efficiency during cycling exercise (28), as previously reported in young subjects with a greater percentage of type I muscle fibers (6). The second difference between the studies that have reported decreased rather than increased mechanical efficiency with age is exercise modality: Dr. Ortega et al. (21), as well other studies (12, 20), demonstrated a significantly reduced efficiency during walking in ∼75-year-old subjects. However, as recognized by the authors, this reduced efficiency exhibited by older subjects is likely caused by the utilization of ancillary muscles during walking and may not be a consequence of muscular metabolic efficiency itself. In contrast, somewhat more simple exercise such as cycling or knee extension appear to be more appropriate models with which to assess skeletal muscle mechanical efficiency, as these paradigms are less biased by both technique and the recruitment of additional muscles not directly involved in the exercise.In summary, aging results in a progressive shift in skeletal muscle phenotype resulting in a greater fraction of type I muscle fibers. As type I fibers exhibit a greater metabolic efficiency and altered activation patterns it is likely that this translates to a greater skeletal muscle mechanical efficiency with advancing age.REFERENCES1. Allman BL , Rice CL. An age-related shift in the force-frequency relationship affects quadriceps fatigability in old adults. J Appl Physiol 96: 1026–1032, 2004.Link | ISI | Google Scholar2. Bell MP , Ferguson RA. Interaction between muscle temperature and contraction velocity affects mechanical efficiency during moderate-intensity cycling exercise in young and older women. J Appl Physiol 107: 763–769, 2009.Link | ISI | Google Scholar3. Buford TW , Lott DJ , Marzetti E , Wohlgemuth SE , Vandenborne K , Pahor M , Leeuwenburgh C , Manini TM. Age-related differences in lower extremity tissue compartments and associations with physical function in older adults. Exp Gerontol 47: 38–44, 2012.Crossref | ISI | Google Scholar4. Chung LH , Callahan DM , Kent-Braun JA. Age-related resistance to skeletal muscle fatigue is preserved during ischemia. J Appl Physiol 103: 1628–1635, 2007.Link | ISI | Google Scholar5. Conley KE , Amara CE , Jubrias SA , Marcinek DJ. Mitochondrial function, fibre types and ageing: new insights from human muscle in vivo. Exp Physiol 92: 333–339, 2007.Crossref | PubMed | ISI | Google Scholar6. Coyle EF , Sidossis LS , Horowitz JF , Beltz JD. Cycling efficiency is related to the percentage of type I muscle fibers. Med Sci Sports Exerc 24: 782–788, 1992.Crossref | PubMed | ISI | Google Scholar7. Crow MT , Kushmerick MJ. Chemical energetics of slow- and fast-twitch muscles of the mouse. J Gen Physiol 79: 147–166, 1982.Crossref | PubMed | ISI | Google Scholar8. Gaesser GA , Brooks GA. Muscular efficiency during steady-rate exercise: effects of speed and work rate. J Appl Physiol 38: 1132–1139, 1975.Link | ISI | Google Scholar9. He ZH , Bottinelli R , Pellegrino MA , Ferenczi MA , Reggiani C. ATP consumption and efficiency of human single muscle fibers with different myosin isoform composition. Biophys J 79: 945–961, 2000.Crossref | PubMed | ISI | Google Scholar10. Hepple RT , Hagen JL , Krause DJ , Baker DJ. Skeletal muscle aging in F344BN F1-hybrid rats: II. Improved contractile economy in senescence helps compensate for reduced ATP-generating capacity. J Gerontol A Biol Sci Med Sci 59: 1111–1119, 2004.Crossref | PubMed | ISI | Google Scholar11. Hook P , Sriramoju V , Larsson L. Effects of aging on actin sliding speed on myosin from single skeletal muscle cells of mice, rats, and humans. Am J Physiol Cell Physiol 280: C782–C788, 2001.Link | ISI | Google Scholar12. Hortobagyi T , Finch A , Solnik S , Rider P , DeVita P. Association between muscle activation and metabolic cost of walking in young and old adults. J Gerontol A Biol Sci Med Sci 66: 541–547, 2011.Crossref | PubMed | ISI | Google Scholar13. Hunter GR , Newcomer BR , Larson-Meyer DE , Bamman MM , Weinsier RL. Muscle metabolic economy is inversely related to exercise intensity and type II myofiber distribution. Muscle Nerve 24: 654–661, 2001.Crossref | PubMed | ISI | Google Scholar14. Jackman MR , Willis WT. Characteristics of mitochondria isolated from type I and type IIb skeletal muscle. Am J Physiol Cell Physiol 270: C673–C678, 1996.Link | ISI | Google Scholar15. Korhonen MT , Cristea A , Alen M , Hakkinen K , Sipila S , Mero A , Viitasalo JT , Larsson L , Suominen H. Aging, muscle fiber type, and contractile function in sprint-trained athletes. J Appl Physiol 101: 906–917, 2006.Link | ISI | Google Scholar16. Lanza IR , Russ DW , Kent-Braun JA. Age-related enhancement of fatigue resistance is evident in men during both isometric and dynamic tasks. J Appl Physiol 97: 967–975, 2004.Link | ISI | Google Scholar17. Lawrenson L , Poole JG , Kim J , Brown C , Patel P , Richardson RS. Vascular and metabolic response to isolated small muscle mass exercise: effect of age. Am J Physiol Heart Circ Physiol 285: H1023–H1031, 2003.Link | ISI | Google Scholar18. Lexell J. Human aging, muscle mass, and fiber type composition. J Gerontol A Biol Sci Med Sci 50 Spec No: 11–16, 1995.PubMed | ISI | Google Scholar19. Lexell J , Taylor CC , Sjostrom M. What is the cause of the ageing atrophy? Total number, size and proportion of different fiber types studied in whole vastus lateralis muscle from 15- to 83-year-old men. J Neurol Sci 84: 275–294, 1988.Crossref | PubMed | ISI | Google Scholar20. Mian OS , Thom JM , Ardigo LP , Narici MV , Minetti AE. Metabolic cost, mechanical work, and efficiency during walking in young and older men. Acta Physiol (Oxf) 186: 127–139, 2006.Crossref | PubMed | ISI | Google Scholar21. Ortega JD , Farley CT. Individual limb work does not explain the greater metabolic cost of walking in elderly adults. J Appl Physiol 102: 2266–2273, 2007.Link | ISI | Google Scholar22. Poole DC , Gaesser GA , Hogan MC , Knight DR , Wagner PD. Pulmonary and leg VO2 during submaximal exercise: implications for muscular efficiency. J Appl Physiol 72: 805–810, 1992.Link | ISI | Google Scholar23. Schiaffino S , Reggiani C. Fiber types in mammalian skeletal muscles. Physiol Rev 91: 1447–1531, 2011.Link | ISI | Google Scholar24. Smith JM , Van Ness HCja. Introduction to Chemical Engineering Thermodynamics. New York: McGraw-Hill, 2000.Google Scholar25. Stienen GJ , Kiers JL , Bottinelli R , Reggiani C. Myofibrillar ATPase activity in skinned human skeletal muscle fibres: fibre type and temperature dependence. J Physiol 493: 299–307, 1996.Crossref | PubMed | ISI | Google Scholar26. Szentesi P , Zaremba R , van Mechelen W , Stienen GJ. ATP utilization for calcium uptake and force production in different types of human skeletal muscle fibres. J Physiol 531: 393–403, 2001.Crossref | PubMed | ISI | Google Scholar27. Tevald MA , Foulis SA , Lanza IR , Kent-Braun JA. Lower energy cost of skeletal muscle contractions in older humans. Am J Physiol Regul Integr Comp Physiol 298: R729–R739, 2010.Link | ISI | Google Scholar28. Venturelli M , Schena F , Scarsini R , Muti E , Richardson RS. Limitations to exercise in female centenarians: evidence that muscular efficiency tempers the impact of failing lungs. Age (Dordr). In press.Google Scholar29. Wendt IR , Gibbs CL. Energy production of rat extensor digitorum longus muscle. Am J Physiol 224: 1081–1086, 1973.Link | ISI | Google ScholarSupplemental datadescriptions.docx (5.18 kb) Download PDF Previous Back to Top Next FiguresReferencesRelatedInformation Cited ByCycling efficiency and energy cost of walking in young and older adultsGlenn A. Gaesser, Wesley J. Tucker, Brandon J. Sawyer, Dharini M. Bhammar, andSiddhartha S. 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