|Year : 2021 | Volume
| Issue : 3 | Page : 93-98
Use it or lose it – Sarcopenia and physical activity
Final Year Medical Student, Stanley Medical College, Chennai, Tamil Nadu, India
|Date of Submission||14-Aug-2021|
|Date of Decision||06-Dec-2021|
|Date of Acceptance||27-Nov-2021|
|Date of Web Publication||16-Dec-2021|
Stanley Medical College Ladies Hostel, Old Jail Road, Royapuram, Chennai - 600 001, Tamil Nadu
Source of Support: None, Conflict of Interest: None
Sarcopenia is a geriatric disease characterized by a marked loss of muscle mass and strength. This has led to it being recognized for the role it plays in elderly morbidity and mortality. It is a multifactorial disease with many mechanisms to how it comes about. So far, increasing physical activity has proven to be the best therapeutic agent. Exercise is capable of increasing flow of nutrition to muscle, reversing mitochondrial damage, increasing muscle mass, and strength. Furthermore, resistance training has been shown to be superior to aerobic training when it comes to increasing muscle mass and strength. Additionally, exercise plays a role in both prevention and treatment of sarcopenia, especially in a background of adequate nutrition. With increasing age, the effect of exercise is also subjected to issues such as anabolic resistance that can make increasing muscle mass and strength more challenging. However, physical activity and exercise remain the most important components of improving muscular strength.
Keywords: Aged, exercise, muscle strength, resistance training, sarcopenia
|How to cite this article:|
Rudra S. Use it or lose it – Sarcopenia and physical activity. J Indian Acad Geriatr 2021;17:93-8
| Introduction|| |
The term sarcopenia was introduced in 1989 by Rosenberg to define the age-related loss of muscle mass and it was not until 2016 that this disease was added to the ICD-10. It became recognized as a separate disease that specifically affects the elderly. The European Working Group on Sarcopenia in Older People (EWGSOP) and the Asian Working Group for Sarcopenia (AWGS) define sarcopenia as a disease characterized by low muscle strength and decreased muscle.,
Studies have shown that decreasing physical activity and age-associated hormonal, neurological, and inflammatory changes play a role in the development of sarcopenia.
It puts those affected at a greater risk of falls, lower quality of life, depression, and mortality., It is common in hospitalized patients and is a predictor of an increased risk of poor outcomes., This makes sarcopenia especially relevant today as COVID-19 has largely kept everyone, including most older adults at home under lockdown decreasing their physical activity levels.
Studies looking into preventing and treating sarcopenia most commonly explore resistance exercise and nutrition supplementation with protein, in isolation or in combination. This paper aims to describe the role that exercise plays in preventing, regressing, or reversing sarcopenia.
| Mechanisms of Sarcopenia|| |
The physiological process of aging results in a gradual loss of muscle mass which is in turn the cause of a reduced basal metabolic rate in older adults. This process is slow and variable in individuals but is inevitable regardless of how active one might be. Type II fast-twitch muscle fibers which have a faster response than type I fibers experience the most loss, but it has been demonstrated that muscle plasticity is retained well into old age.
There are various factors contributing to this disease including low levels of anabolic hormones, increases in inflammation, inactivity/immobilization, change in muscle fiber type, neuromuscular change, oxidative stress, mitochondrial damage, and genetics.
Aging leads to a fall in growth hormone and testosterone, both well-known anabolic hormones that promote muscle growth. Muscle loss after a fall in estrogen in women is more likely due to the loss of estrogen's ability to prevent autophagy of skeletal muscle.
Perhaps, one of the most important contributors is inactivity. Bed rest studies have shown accelerated muscle loss in those with prolonged hospital stays., In a study by Justine et al., elderly adults spent less hours engaging in physical activity due to external barriers, citing reasons such as “not having enough time.” Disuse may be a greater contributor to muscle loss than the process of aging itself.
Changes to insulin-like growth factor-1 (IGF-1) signaling of mammalian target of rapamycin (mTOR) and Akt pathway are contributory. Muscle growth occurs when IGF-1 acts via the Akt/mTOR pathway to increase protein synthesis. With age, there is a decreased sensitivity to insulin and IGF-1 termed “anabolic resistance.”
The term “inflammaging” describes the state of chronic low-grade inflammation in the elderly. Inflammation marked by high C-reactive protein (CRP) levels has also been shown to be associated with a decrease in muscle strength., Additionally, visceral fat also contributes to inflammation which in turn encourages muscle loss, as seen in sarcopenic obesity. The elderly are more likely to experience comorbidities which result in higher amounts of proinflammatory cytokines having a detrimental effect on their skeletal muscle.,,
Neurological changes at various levels from the central nervous system down to the neuromuscular junction may be a contributor to sarcopenia. Other factors such as increased oxidative stress, mitochondrial damage, dysfunction of satellite cells which reduces protein synthesis, and genetics may increase the likelihood of developing sarcopenia.
Sarcopenia is a multifactorial process, and overall, it can be seen that anabolism declines in the elderly. Physical activity may be able to slow or reverse the effects of some of these processes. Physical activity and the types of exercises that could be employed and their role in sarcopenia are reviewed below.
| Physical Activity|| |
Physical activity was defined by Caspersen et al. as “any bodily movement produced by skeletal muscles that result in energy expenditure.” Whereas exercise is defined as “physical activity that is planned, structured, repetitive, and purposive.” By this definition, fidgeting may also be characterized as a physical activity, though it does not lead to the same benefits as exercise does.
Physical activity may be categorized based on intensity or metabolic equivalent of task (MET). 1 MET is defined as the energy required to sit quietly which is approximately 3.5 mL of oxygen per kilogram of body weight. If a task is 3 METs, then it requires three times the energy than that of sitting quietly. Sedentary behavior is 1.0–1.5 METs, light activity is 1.6–2.9 METs, moderate activity is 3.0–5.9 METs, and vigorous activity is ≥6.0 METs.
Physical activity recommendations for older adults include four different components, namely aerobic exercise, resistance training, balance, and flexibility.
| Aerobic Exercise|| |
Aerobic exercise is any physical activity that relies on oxygen for the production of energy.
Aerobic exercise has long been considered one of the best ways to improve mitochondrial mass in cells. It has shown a reduction in mitochondrial damage and is even able to reverse some mitochondrial dysfunction, all of which are implicated as a causative factor of sarcopenia. Additionally, aerobic exercise also works in favor of reducing inflammation seen by decreased CRP levels in those who regularly take part in aerobic exercise. As with mitochondrial damage, inflammation too has a role to play in those who develop sarcopenia.
Apart from these benefits, aerobic exercise improves cardiovascular health, lung capacity, metabolic profiles, mental health, and overall quality of life.,,
Some forms of aerobic exercise are jogging, brisk walking, Nordic walking, cycling, dancing, etc.
| Resistance Training|| |
Resistance training is a form of exercise that requires muscles to work against a weight. This may be an external weight such as a dumbbell or even bodyweight.
Resistance training increases muscle mass and strength, which are greatly reduced in sarcopenia.
Resistance training has been known to induce muscle hypertrophy over a period of time with an increase in type II fibers. This effect appears to be less pronounced in older people due to less capillarization of their muscles. Decreased capillarization results in suboptimal delivery of nutrient and oxygen to the muscles. Some studies have shown that resistance training itself can increase capillarization while others maintain that aerobic exercise is the most reliable method to increase angiogenic response. Adding aerobic exercise to a program before resistance training could provide optimal results.
Jubrias et al. showed that resistance training is more effective than aerobic exercise at increasing mitochondrial biogenesis, and Taivassalo et al. showed that mitochondrial biogenesis is similar regardless of mode of exercise.,, In addition to improving muscle health, it has a positive effect on bone density and cardiovascular health, and metabolic profile.
These benefits are dependent on some aspects of the resistance training program such as volume, intensity, frequency, and progressive overload.
Volume is defined as the amount of exercise done. This is measured using the number of sets, repetitions, and load (external or bodyweight). For example, if one does 3 sets of 10 repetitions at 5 kg, the load is 3 × 10 × 5 = 150 kg.
Intensity is usually taken as the percentage of one's maximum load at which they can perform 1 repetition, or the 1 repetition maximum. This definition has been challenged, and it is suggested that intensity rather be taken as “the effort applied to a load.” In older adults, a more subjective approach to measuring intensity is taken that requires older adults to point out their level of effort on a scale of 0–10, 0 being no effort and 10 being maximal effort. Moderate intensity is rated at 5–6 and high intensity is 7–8.
The frequency is how often a resistance training routine is implemented in a week.
Progressive overload is the measured increase in stress placed on the muscles, necessary to keep stimulating the muscles to grow. This can be achieved in various ways by increasing the repetitions, the load, intensity, or frequency. Progressive overload is done slowly over a long period giving the body time to adapt and then overloading it to create more stimuli for growth.
Some examples of resistance training are bodyweight exercises or calisthenics, free weights, elastic resistance bands, or machine weights.
Keeping these principles in mind, resistance training programs are designed for older adults.
| Balance and Flexibility|| |
Sarcopenic adults are more prone to losing balance and falling. Practicing exercises that help build more balance is important in this group, though studies have not looked into balance training alone in this group.
Flexibility increases the range of motion of joints and helps prevent injuries as older populations often lose flexibility with age.
Examples of such exercises include unilateral training, yoga, and tai chi.
| Physical Activity as Prevention of Sarcopenia|| |
Inactivity is a modifiable risk factor of sarcopenia. Prevention of sarcopenia is still an area for more research, and the role of nutrition and exercise is investigated the most in this regard. Ideally, prevention should start early in life by increasing physical activity and optimizing nutrition, but it remains a question whether it is ever too late to prevent sarcopenia by exercise.
Resistance training is regarded as the best way to gain muscle mass and build strength. A recent umbrella review of systematic reviews has shown that low-intensity resistance training is enough to increase muscular strength, but results of high-intensity training were even better.
Hong et al. explored the changes resistance training would bring about in different sarcopenic parameters in 12 weeks. They found that lower body mass increased but not the upper-body mass. Total appendicular lean soft tissue and total skeletal mass increased as well. Strength did not increase. This may be due to the fewer number of sets and repetitions than recommended by the American College of Sports Medicine and the American Heart Association.
Vikberg et al. too showed an increase in muscle mass in presarcopenic adults who underwent the 10-week resistance training program. The increase in lower body strength was limited to the males in the exercise group. There was an improvement in sit-to-stand test of those who underwent training. Participants were given an optional protein supplement. Eighty-four percent of participants took the supplement, and not having a separate group with and without supplements apart from the control group makes the true analysis of the effect of training on presarcopenic population difficult.
Another study of a 6-week training program in older women showed an increase in muscle strength and quality.
Martins et al. have shown beneficial results of using elastic resistance bands to increase muscle mass and strength. This may be considered as it is a cheaper, safer, and easier to use at home alternative than traditional free weights.
Aerobic exercise is not considered the mainstay of increasing muscular mass or strength, but it has shown the ability to increase nutrient delivery to muscles and in turn promote an anabolic response. Robinson et al. studied the effect of 6 weeks of aerobic training in older adults and saw an increase in muscle protein synthesis and DNA when compared to a younger sedentary group. Lustosa et al. compared the effects of combined aerobic and resistance training to resistance training alone in older adults at risk of sarcopenia according to the EWGSOP criteria. The study found that both groups exhibited improvements in balance and mobility, but the combined exercise group showed greater improvements than the group doing resistance training alone. Aerobic training could also have a place in improving muscle health in older adults.
More long-term studies are required to see the extent of muscular strength gains that can be made in older adults with and without presarcopenia. Older adults can be studied for the developement of sarcopenia in exercise and non-exercise groups, to understand if sarcopenia can be prevented in them and to what extent.
| Physical Activity as Intervention in Sarcopenia|| |
Several studies have shown the benefits of exercise on healthy aging muscles. But can the same effects be translated onto someone with a diagnosis of sarcopenia?
Resistance exercise exceeds aerobic exercise when it comes to increasing both muscle mass and strength. The beneficial effects have been noticed in as little as 8 weeks' time. Other studies done over 12 weeks showed improvements in muscle mass with strength training.,
Piastra et al. conducted a 9-month long study on community-dwelling sarcopenic women. They were diagnosed based on the EWGSOP criteria; the intervention group underwent low-intensity resistance training twice a week for 60 min. The other group underwent postural training alone. The participants in the intervention group went from being classified as “moderate” sarcopenic to “normal” according to the EWGSOP criteria. In addition to this, there were significant improvements in balance, muscle mass, skeletal muscle index, and handgrip strength.
Another study investigated the effects of 8-week resistance training program on sarcopenic women. They were diagnosed by the AWGS criteria; the intervention group did moderate-intensity resistance training using a kettlebell as the external load. Training was conducted twice a week for 60 min. Grip strength and appendicular skeletal mass increased in the intervention group. Moreover, the participants were studied at week 12, which provided them with 4 weeks of detraining. The results were that even after detraining, these effects were significantly higher than before the start of training. On the other hand, the control group showed deteriorating skeletal mass as it was lower at weeks 8 and 12 than at week 0. The results also showed increased lung capacity and lower CRP levels.
Zhu et al. implemented a 12-week exercise and nutrition program in community-dwelling sarcopenic individuals diagnosed by the AWGS criteria. There were four groups: exercise alone, exercise and nutrition, nutrition alone, and no intervention group. The exercise group would perform resistance training using elastic bands and aerobic exercises in each session. The nutrition group was provided with 2 packs of supplements to take daily containing 231 calories each along with 8.61 g protein, 1.21 g β-hydroxy β-methylbutyrate, 130 IU Vitamin D, and 0.29 g omega-3 fatty acid. The results showed that muscle mass was significantly higher in the nutrition and exercise group, but strength gains were higher in the exercise group regardless of nutritional supplement intake. The primary outcome of gait speed had not improved. This may be attributed to the short nature of the study or that use of elastic band as resistance instead of a heavier load. The participants were followed up 12 weeks later, and the exercise groups were given elastic bands and exercise booklet to continue their training at home. The strength gains were maintained at week 24, but muscle mass was not. This shows that muscle mass may be more sensitive to dietary changes than muscle strength is. Muscle strength is a better indicator of outcomes in sarcopenia than muscle mass, so exercising cannot be replaced by diet to maintain strength. However, diet plays an essential role in gain, loss, and maintenance of muscle mass. Another study investigating the relationship of nutrition and exercise in sarcopenic adults showed that collagen peptide supplementation in combination with exercise increased muscle strength more than the group doing exercise alone. Kim et al. concluded that exercise and essential amino acid supplementation together increased both strength and mass, but exercise alone only increased muscle mass. These studies have varying results, but Zhu et al. performing a follow-up provided some more insight into the strength and mass changes after the withdrawal of any intervention.
So far, it appears that exercise has a net positive effect on community-dwelling sarcopenic individuals, but sarcopenia is also very common in hospitalized individuals. Wang et al. studied the effects of a short-term, 2-week exercise program on hospitalized sarcopenia patients. They were diagnosed using the AWGS criteria, and the intervention group underwent mixed training including resistance, aerobic, and balance for 5 days a week for 60 min a day excluding warm-up. After the 2 weeks, the exercise group had higher activities of daily living score and increased gait speed. There were no significant changes to strength parameters. This could be due to the short-term nature of the study. Could strength need more time to develop? In the hospitalized elderly do other factors such as higher inflammation, reduced ambulation, inability to perform exercise with correct posture, and comorbidities increase the time it may take to gain strength?
It is possible that anabolic resistance in some sarcopenic individuals may make exercise a less than fruitful intervention. Kumar et al. demonstrated an age-dependent change in response of muscle synthesis to resistance exercise. Additionally, neurological damage in others may make muscle recruitment and strength and also increase the challenge. Exercising has been proven to be effective in increasing anabolic hormones and against “inflammaging.”, Group training can be investigated to see if it encourages older adults to be less inactive.
Studies that investigate a more standardized exercise intervention and multimodal training in those with sarcopenia are still limited. Such studies will put us on the path to specify recommendations for type of exercise, and the dose and frequency for treating sarcopenia.
| Conclusion|| |
Exercise is an important aspect in improving muscular health to prevent and treat sarcopenia. Resistance training is one of the best ways to do this. Resistance training can also prevent the deterioration of muscle mass and strength that would happen in an otherwise sedentary older adult. Additionally, multimodal training could show promise with more research in the future. Currently, there is no streamlined recommendation on exercise in those with sarcopenia, and this should ideally change with hereafter.
I would like to thank Prof. Alka Ganesh for her guidance in this article.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Irwin H Rosenberg, Summary comments. Am J Clin Nutr 1989;50:1231-33.
Anker SD, Morley JE, von Haehling S. Welcome to the ICD-10 code for sarcopenia. J Cachexia Sarcopenia Muscle 2016;7:512-4.
Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyère O, Cederholm T, et al
. Sarcopenia: Revised European consensus on definition and diagnosis. Age Ageing 2019;48:16-31.
Chen LK, Woo J, Assantachai P, Auyeung TW, Chou MY, Iijima K, et al
. Asian Working Group for Sarcopenia: 2019 consensus update on sarcopenia diagnosis and treatment. J Am Med Dir Assoc 2020;21:300-7.e2.
Burton LA, Sumukadas D. Optimal management of sarcopenia. Clin Interv Aging 2010;5:217-28.
Hayashi T, Umegaki H, Makino T, Cheng XW, Shimada H, Kuzuya M. Association between sarcopenia and depressive mood in urban-dwelling older adults: A cross-sectional study. Geriatr Gerontol Int 2019;19:508-12.
Smoliner C, Sieber CC, Wirth R. Prevalence of sarcopenia in geriatric hospitalized patients. J Am Med Dir Assoc 2014;15:267-72.
Du Y, Karvellas CJ, Baracos V, Williams DC, Khadaroo RG; Acute Care and Emergency Surgery (ACES) Group. Sarcopenia is a predictor of outcomes in very elderly patients undergoing emergency surgery. Surgery 2014;156:521-7.
Parmet WE, Sinha MS. COVID-19 – The law and limits of quarantine. N Engl J Med 2020;382:e28.
Tison GH, Avram R, Kuhar P, Abreau S, Marcus GM, Pletcher MJ, et al
. Worldwide effect of COVID-19 on physical activity: A descriptive study. Ann Intern Med 2020;173:767-70.
Tzankoff SP, Norris AH. Effect of muscle mass decrease on age-related BMR changes. J Appl Physiol Respir Environ Exerc Physiol 1977;43:1001-6.
Korhonen MT, Cristea A, Alén M, Häkkinen K, Sipilä S, Mero A, et al
. Aging, muscle fiber type, and contractile function in sprint-trained athletes. J Appl Physiol (1985) 2006;101:906-17.
Ciciliot S, Rossi AC, Dyar KA, Blaauw B, Schiaffino S. Muscle type and fiber type specificity in muscle wasting. Int J Biochem Cell Biol 2013;45:2191-9.
Paillard T. Muscle plasticity of aged subjects in response to electrical stimulation training and inversion and/or limitation of the sarcopenic process. Ageing Res Rev 2018;46:1-13.
Brotto M, Abreu EL. Sarcopenia: Pharmacology of today and tomorrow. J Pharmacol Exp Ther 2012;343:540-6.
Collins BC, Laakkonen EK, Lowe DA. Aging of the musculoskeletal system: How the loss of estrogen impacts muscle strength. Bone 2019;123:137-44.
Ikezoe T, Mori N, Nakamura M, Ichihashi N. Effects of age and inactivity due to prolonged bed rest on atrophy of trunk muscles. Eur J Appl Physiol 2012;112:43-8.
Kortebein P, Ferrando A, Lombeida J, Wolfe R, Evans WJ. Effect of 10 days of bed rest on skeletal muscle in healthy older adults. JAMA 2007;297:1772-4.
Justine M, Azizan A, Hassan V, Salleh Z, Manaf H. Barriers to participation in physical activity and exercise among middle-aged and elderly individuals. Singapore Med J 2013;54:581-6.
Peterson MD, Rhea MR, Sen A, Gordon PM. Resistance exercise for muscular strength in older adults: A meta-analysis. Ageing Res Rev 2010;9:226-37.
Barclay RD, Burd NA, Tyler C, Tillin NA, Mackenzie RW. The role of the IGF-1 signaling cascade in muscle protein synthesis and anabolic resistance in aging skeletal muscle. Front Nutr 2019;6:146.
Franceschi C, Bonafè M, Valensin S, Olivieri F, De Luca M, Ottaviani E, et al
. Inflamm-aging. An evolutionary perspective on immunosenescence. Ann N Y Acad Sci 2000;908:244-54.
Tuttle CS, Thang LA, Maier AB. Markers of inflammation and their association with muscle strength and mass: A systematic review and meta-analysis. Ageing Res Rev 2020;64:101185.
Schaap LA, Pluijm SM, Deeg DJ, Harris TB, Kritchevsky SB, Newman AB, et al
. Higher inflammatory marker levels in older persons: Associations with 5-year change in muscle mass and muscle strength. J Gerontol A Biol Sci Med Sci 2009;64:1183-9.
Choi KM. Sarcopenia and sarcopenic obesity. Korean J Intern Med 2016;31:1054-60.
Byun MK, Cho EN, Chang J, Ahn CM, Kim HJ. Sarcopenia correlates with systemic inflammation in COPD. Int J Chron Obstruct Pulmon Dis 2017;12:669-75.
Kim JK, Choi SR, Choi MJ, Kim SG, Lee YK, Noh JW, et al
. Prevalence of and factors associated with sarcopenia in elderly patients with end-stage renal disease. Clin Nutr 2014;33:64-8.
Brinkley TE, Leng X, Miller ME, Kitzman DW, Pahor M, Berry MJ, et al
. Chronic inflammation is associated with low physical function in older adults across multiple comorbidities. J Gerontol A Biol Sci Med Sci 2009;64:455-61.
Kwon YN, Yoon SS. Sarcopenia: Neurological point of view. J Bone Metab 2017;24:83-9.
Marzetti E, Calvani R, Cesari M, Buford TW, Lorenzi M, Behnke BJ, et al
. Mitochondrial dysfunction and sarcopenia of aging: From signaling pathways to clinical trials. Int J Biochem Cell Biol 2013;45:2288-301.
Urzi F, Pokorny B, Buzan E. Pilot study on genetic associations with age-related sarcopenia. Front Genet 2020;11:615238.
Doherty TJ. Invited review: Aging and sarcopenia. J Appl Physiol (1985) 2003;95:1717-27.
Caspersen CJ, Powell KE, Christenson GM. Physical activity, exercise, and physical fitness: Definitions and distinctions for health-related research. Public Health Rep 1985;100:126-31.
Ainsworth BE, Haskell WL, Herrmann SD, Meckes N, Bassett DR Jr., Tudor-Locke C, et al
. 2011 compendium of physical activities: A second update of codes and MET values. Med Sci Sports Exerc 2011;43:1575-81.
Sparling PB, Howard BJ, Dunstan DW, Owen N. Recommendations for physical activity in older adults. BMJ 2015;350:h100.
Nilsson MI, Tarnopolsky MA. Mitochondria and aging – The role of exercise as a countermeasure. Biology (Basel) 2019;8:E40.
Zheng G, Qiu P, Xia R, Lin H, Ye B, Tao J, et al
. Effect of aerobic exercise on inflammatory markers in healthy middle-aged and older adults: A systematic review and meta-analysis of randomized controlled trials. Front Aging Neurosci 2019;11:98.
Park J, Han D. Effects of high intensity aerobic exercise on treadmill on maximum-expiratory lung capacity of elderly women. J Phys Ther Sci 2017;29:1454-7.
Chapman SB, Aslan S, Spence JS, Defina LF, Keebler MW, Didehbani N, et al
. Shorter term aerobic exercise improves brain, cognition, and cardiovascular fitness in aging. Front Aging Neurosci 2013;5:75.
Finucane FM, Sharp SJ, Purslow LR, Horton K, Horton J, Savage DB, et al
. The effects of aerobic exercise on metabolic risk, insulin sensitivity and intrahepatic lipid in healthy older people from the Hertfordshire Cohort Study: A randomised controlled trial. Diabetologia 2010;53:624-31.
American College of Sports Medicine; Chodzko-Zajko WJ, Proctor DN, Fiatarone Singh MA, Minson CT, Nigg CR, et al
. American College of Sports Medicine position stand. Exercise and physical activity for older adults. Med Sci Sports Exerc 2009;41:1510-30.
Csapo R, Alegre LM. Effects of resistance training with moderate vs. heavy loads on muscle mass and strength in the elderly: A meta-analysis. Scand J Med Sci Sports 2016;26:995-1006.
Snijders T, Nederveen JP, Bell KE, Lau SW, Mazara N, Kumbhare DA, et al
. Prolonged exercise training improves the acute type II muscle fibre satellite cell response in healthy older men. J Physiol 2019;597:105-19.
Snijders T, Nederveen JP, Joanisse S, Leenders M, Verdijk LB, van Loon LJ, et al
. Muscle fibre capillarization is a critical factor in muscle fibre hypertrophy during resistance exercise training in older men. J Cachexia Sarcopenia Muscle 2017;8:267-76.
Jubrias SA, Esselman PC, Price LB, Cress ME, Conley KE. Large energetic adaptations of elderly muscle to resistance and endurance training. J Appl Physiol (1985) 2001;90:1663-70.
Taivassalo T, Fu K, Johns T, Arnold D, Karpati G, Shoubridge EA. Gene shifting: A novel therapy for mitochondrial myopathy. Hum Mol Genet 1999;8:1047-52.
Schoenfeld BJ, Wilson JM, Lowery RP, Krieger JW. Muscular adaptations in low- versus high-load resistance training: A meta-analysis. Eur J Sport Sci 2016;16:1-10.
Mangine GT, Hoffman JR, Gonzalez AM, Townsend JR, Wells AJ, Jajtner AR, et al
. The effect of training volume and intensity on improvements in muscular strength and size in resistance-trained men. Physiol Rep 2015;3:e12472.
Fisher J, Smith D. Attempting to better define “intensity” for muscular performance: Is it all wasted effort? Eur J Appl Physiol 2012;112:4183-5.
Nelson ME, Rejeski WJ, Blair SN, Duncan PW, Judge JO, King AC, et al
. Physical activity and public health in older adults: Recommendation from the American College of Sports Medicine and the American Heart Association. Med Sci Sports Exerc 2007;39:1435-45.
Kraemer WJ, Ratamess NA, French DN. Resistance training for health and performance. Curr Sports Med Rep 2002;1:165-71.
Dennison EM, Sayer AA, Cooper C. Epidemiology of sarcopenia and insight into possible therapeutic targets. Nat Rev Rheumatol 2017;13:340-7.
Beckwée D, Delaere A, Aelbrecht S, Baert V, Beaudart C, Bruyere O, et al
. Exercise interventions for the prevention and treatment of sarcopenia. A systematic umbrella review. J Nutr Health Aging 2019;23:494-502.
Hong J, Kim J, Kim SW, Kong HJ. Effects of home-based tele-exercise on sarcopenia among community-dwelling elderly adults: Body composition and functional fitness. Exp Gerontol 2017;87:33-9.
Vikberg S, Sörlén N, Brandén L, Johansson J, Nordström A, Hult A, et al
. Effects of resistance training on functional strength and muscle mass in 70-year-old individuals with pre-sarcopenia: A randomized controlled trial. J Am Med Dir Assoc 2019;20:28-34.
Pinto RS, Correa CS, Radaelli R, Cadore EL, Brown LE, Bottaro M. Short-term strength training improves muscle quality and functional capacity of elderly women. Age (Dordr) 2014;36:365-72.
Martins WR, de Oliveira RJ, Carvalho RS, de Oliveira Damasceno V, da Silva VZ, Silva MS. Elastic resistance training to increase muscle strength in elderly: A systematic review with meta-analysis. Arch Gerontol Geriatr 2013;57:8-15.
Timmerman KL, Dhanani S, Glynn EL, Fry CS, Drummond MJ, Jennings K, et al
. A moderate acute increase in physical activity enhances nutritive flow and the muscle protein anabolic response to mixed nutrient intake in older adults. Am J Clin Nutr 2012;95:1403-12.
Robinson MM, Turner SM, Hellerstein MK, Hamilton KL, Miller BF. Long-term synthesis rates of skeletal muscle DNA and protein are higher during aerobic training in older humans than in sedentary young subjects but are not altered by protein supplementation. FASEB J 2011;25:3240-9.
Lustosa LP, Pereira DAG, Parentoni AN, Dias RC, Dias JMD, et al
. Impact of aerobic training associated with muscle strengthening in elderly individuals at risk of sarcopenia: A clinical trial. J Gerontol Geriat Res 2015;4:208. doi:10.4172/2167-7182.1000208.
Chen HT, Wu HJ, Chen YJ, Ho SY, Chung YC. Effects of 8-week kettlebell training on body composition, muscle strength, pulmonary function, and chronic low-grade inflammation in elderly women with sarcopenia. Exp Gerontol 2018;112:112-8.
Zhu LY, Chan R, Kwok T, Cheng KC, Ha A, Woo J. Effects of exercise and nutrition supplementation in community-dwelling older Chinese people with sarcopenia: A randomized controlled trial. Age Ageing 2019;48:220-8.
Kim HK, Suzuki T, Saito K, Yoshida H, Kobayashi H, Kato H, et al
. Effects of exercise and amino acid supplementation on body composition and physical function in community-dwelling elderly Japanese sarcopenic women: A randomized controlled trial. J Am Geriatr Soc 2012;60:16-23.
Piastra G, Perasso L, Lucarini S, Monacelli F, Bisio A, Ferrando V, et al
. Effects of two types of 9-month adapted physical activity program on muscle mass, muscle strength, and balance in moderate sarcopenic older women. Biomed Res Int 2018;2018:5095673.
Zdzieblik D, Oesser S, Baumstark MW, Gollhofer A, König D. Collagen peptide supplementation in combination with resistance training improves body composition and increases muscle strength in elderly sarcopenic men: A randomised controlled trial. Br J Nutr 2015;114:1237-45.
Wang R, Liang Y, Jiang J, Chen M, Li L, Yang H, et al
. Effectiveness of a short-term mixed exercise program for treating sarcopenia in hospitalized patients aged 80 years and older: A prospective clinical trial. J Nutr Health Aging 2020;24:1087-93.
Kumar V, Selby A, Rankin D, Patel R, Atherton P, Hildebrandt W, et al
. Age-related differences in the dose-response relationship of muscle protein synthesis to resistance exercise in young and old men. J Physiol 2009;587:211-7.
Ravaglia G, Forti P, Maioli F, Pratelli L, Vettori C, Bastagli L, et al
. Regular moderate intensity physical activity and blood concentrations of endogenous anabolic hormones and thyroid hormones in aging men. Mech Ageing Dev 2001;122:191-203.