Review
The etiology and exercise implications of
sarcopenia in the elderly
Jie Yu
School of Nursing, Azusa Pacific University, 91702 Azusa, CA, USA
a r t i c l e i n f o
Article history:Received 12 August 2014 Received in revised form 27 April 2015
Accepted 29 April 2015 Available online 9 May 2015 Keywords:
Sarcopenia Resistance exercise Older adults
a b s t r a c t
An increasing aging population greatly impacts health care services worldwide. A large percentage of healthcare expenditures for seniors arise from the negative outcomes of muscle loss, also known as sarcopenia. Aging-related losses of muscle strength and quality impair balance, walking ability and endurance and cause negative events such as falls, incident disability and frailty. This review systemically explores the significance of copenia in the elderly and addresses several important physiological mechanisms of sar-copenia. The implications of crucial exercise regimens that improve muscle strength and delay the onset of sarcopenia are also discussed.
Copyright© 2015, Chinese Nursing Association. Production and hosting by Elsevier (Singapore) Pte Ltd. This is an open access article under the CC BY-NC-ND license (http:// creativecommons.org/licenses/by-nc-nd/4.0/).
A rapidly expanding aging population is one of the factors that impacts health care services across the globe. According to statistics from the U.S. Bureau of the Census, the number of people who are 65 years or older (seniors) equaled 43.1 million in July 2012, representing 15% of the U.S. population. By 2050, it is projected that there will be about 83.7 million seniors representing almost 20% of the population [1]. Health care expenditures for seniors in the U.S. are expected to increase six-fold by 2040[2]and a high percentage of health care costs for seniors arise from the negative outcomes of lean muscle mass loss[3].
This review explores the impact of sarcopenia, which re-fers to the loss of muscle mass and the decline of muscle quality with increased age[4], on the mobility and indepen-dence of the elderly. The physiological causes of sarcopenia and the implications of exercise regimens to improve muscle strength or to delay sarcopenia are discussed.
1.
Significance of sarcopenia
The term of “sarcopenia” was first introduced in 1989 to
describe a progressive, generalized loss of skeletal muscle mass and accompanying decline in muscle strength and per-formance with increasing age. Sarcopenia is associated with many negative outcomes, such as disability, frailty, comor-bidities, hospital admissions and death[4e6].
The prevalence of sarcopenia with advanced age has been
well-documented. Baumgartner and colleagues [7] utilized
data from a population-based study and analyzed the epide-miology of sarcopenia among the New Mexico elderly. The prevalence of sarcopenia was 13e14% in persons under age 70 and >50% in those older than 80. In a 7.8 year longitudinal study, Forbes and Reina[8]reported an average loss of 0.25 kg/ year of lean muscle mass among the participants aged 22e53.
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The significant consequences of sarcopenia have also been well-recognized. Roubenoff [9] investigated the close rela-tionship between muscle mass and strength and found that sarcopenia was important in functional deterioration, including declines in gait and balance, increased fall risks, and loss of independence[10]. Murphy and colleagues[11] exam-ined the time-course of sarcopenia determinants and found that low functioning, lack of physical activity and a high body mass index predicted transition toward sarcopenia, which was more likely to lead to death. Szulc and associates[12]assessed the degree of sarcopenia by the relative appendicular skeletal muscle (RASM) mass index. They found that a decreased RASM value among elderly men was associated with a lower bending strength. Therefore, the authors concluded that sarcopenia in older men was associated with impaired balance and an increased risk of falling. The relationship between sarcopenia and functional status was also investigated in the New Mexico Study7, which revealed that people with sarcopenia had 3e4 fold higher rates of disability, significantly greater risks of falling, and were more likely to use assistive devices[7]. Metter et al.[13]found that sarcopenia could act as a significant pre-dictor of all-cause mortality.
The loss of muscle mass and quality also has metabolic and physiological consequences. Sarcopenia may influence the body's thermoregulation process in both cold and warm
environments [14] and may contribute to age-associated
glucose intolerance[15].
Therefore, sarcopenia not only has detrimental effects on physical functioning, but also impacts skeletal and metabolic health. Sarcopenia greatly diminishes the overall quality of life[3].
2.
Etiology of sarcopenia
Sarcopenia, like many other problems that occur with aging, is a multifactorial condition. Factors that contribute to the occurrence of sarcopenia in the elderly include motor units, protein metabolism, hormones and lifestyle[9].
2.1. Motor units
The loss of alpha motor units from the spinal cord is thought to be the most crucial contributor to sarcopenia[9]. Many studies support this idea. Yuan et al.[16]found from direct micro-scopic observation that the number of motor neurons in the spinal cord decreased with aging. Similarly, McNeil and col-leagues[17]found differences in the number of motor units in the tibialis anterior of young and older men. Their results indicate that age-related motor unit loss may contribute to sarcopenia, but seldom limits mobility or independence until a critical threshold is reached. Concomitant with the decreased number of motor units, the increased size of the remaining motor units and the loss of muscle fibers have also been identified as significant contributing factors to sarcopenia[18].
2.2. Protein metabolism
The balance between protein break down and synthesis rates is crucial in maintaining muscle mass and studies show that
there is a direct relationship between sarcopenia and changes in muscle metabolism. Balagopal et al.[19]found that mixed muscle protein synthesis was reduced by 30% with advanced age. However, the reduction of muscle protein synthesis appeared to be selective. Specifically, whereas synthesis rates of mixed muscle proteins and myosin heavy chains decreased by more than 40% in the elderly; sarcoplasmic protein syn-thesis rates were maintained or increased with age. Several studies have investigated this selectivity, suggesting[20]that it might be due to decreased number sof messenger ribonu-cleic acid (mRNA) for protein translation. Therefore, it is quite likely that the selective decrease in protein synthesis plays an important role in the development of sarcopenia.
2.3. Hormone factors
Many hormones have metabolic effects on muscle mass and function. A convincing body of evidence indicates that the aging process alters the circulating concentrations of several important muscle-building hormones[3]. For brevity, this re-view will concentrate on two important anabolic hormones: testosterone and growth hormone (GH).
2.3.1. Testosterone
Multiple studies indicate that the level of bioavailable free testosterone decreases with age[21]. Specifically, free testos-terone levels decrease approximately 3% per year between the ages of 73 and 94[22]. Additionally, studies show that aging decreases the sensitivity of target tissues, such as muscle, to testosterone [23]. Clinical studies indicate that among the elderly both the decreased level of testosterone and the insensitivity of muscle tissues to testosterone contribute to sarcopenia[24].
2.3.2. Growth hormone (GH)
Since GH is important in muscle mass growth and maintenance, this hormone has been given much attention in recent sarco-penia studies. Multiple studies found that the level of circulating GH decreases with age. For example, Veldhuis and colleagues
[25] found that most of their study participants' GH levels
declined by approximately 50% between the ages of 20 and 70. Some studies have shown a link between the declining GH levels and the loss of muscle mass in the elderly[26]. However, the specific role of the decreased GH levels in sarcopenia occurrence and the feasibility of GH supplementation in sarcopenia man-agement are still unclear and need further investigation.
2.4. Lifestyle factors
It has been well-documented that physical inactivity and mus-cle disuse promote the loss of musmus-cle mass and worsen the degree of sarcopenia[9]. Studies also show that the decline in food intake and protein consumption among the elderly contribute to muscle atrophy and the severity of sarcopenia[21].
3.
Exercise management and implications
Progressive resistance training has long been identified as the most promising imethod for increasing muscle mass and
strength among older people[27,28]. A number of studies have
confirmed the effectiveness of resistance training in
improving muscle mass, strength, balance and endurance among the elderly. For example, Yarasheski and colleagues
[29]found that resistance training could enormously enhance the rate of mixed muscle protein synthesis in physically frail older participants. After three months of weight-lifting exer-cise, the muscle contractile protein synthesis rates in these sedentary seniors were greatly increased. In a randomized and placebo-controlled trial, including nursing home resi-dents, ten weeks of progressive resistance training increased muscle cross sectional area by 3e9% and improved muscle strength and performance in gait speed and stair climbing abilities[30]. Frontera et al.[31]demonstrated that 2 weeks of progressive resistance training could substantially promote extensor and flexor strength in older participants. In evalu-ating muscle protein breakdown during sarcopenia and aging, Fry and associates[32]found that regulators of muscle protein breakdown responded similarly in young and older adults following resistance training, suggesting that resistance training could slow the pace of sarcopenia. Therefore, it is reasonable to conclude from these studues that progressive resistance training could effectively improve or prevent sar-copenia among the elderly, via improvements in muscle mass and strength.
3.1. Implications for exercise prescriptions
When designing a resistance exercise program to manage sarcopenia, some specific guidelines should be addressed. The goal is to gradually overload the muscles and make positive adaptations, such as improvement in muscle mass and function[33]. At the same time, sufficient attention should be paid to specific and normal aging-related physiological in order to avoid exercise-related injuries or severe outcomes.
Generally speaking, a progressive resistance training pro-gram for sarcopenia should be dynamic and target the major muscle groups using both concentric and eccentric move-ments [33]. Exercise program that target lower extremity muscles, such as the knee and hip extensors, should be prioritized because they are important in mobility, balance and gait.
3.1.1. Warm-up and cool-down
Warm-up and cool-down periods should be longer for the elderly [34]. Optimal warm-up activities should last 15e20 minutes, whereas 10e15 minutes should be devoted to the cool-down period. Active muscles should be stretched in both periods, and the warm-up session should involve lifting light weights[35].
3.1.2. Intensity
The intensity of the exercises should be based a combination of parameters, such as the individual's heart rate and energy expenditure[34]. When performing resistance training, the seniors should move the resistance through the entire range of motion and avoid heavy lifting [35]. Specifically, the American College of Sport Medicine (ACMS)[36]recommends resistance training of 65%e75% maximum to increase muscle strength.
3.1.3. Frequency
The guidelines published by ACMS are appropriate to be used among the elderly.
<3 Metabolic Equivalent (MET): 5 minutes of exercise several times daily
3e5 METs: at least twice a day as tolerated 5 METs: 3 times a week on alternate days
ACMS [36] recommends that seniors perform resistance
training 2e4 days per week. Hence, the average frequency should be 3 days per week and the individual should wait at least 48 hours between training sessions.
3.1.4. Duration
ACMS[36]recommends that seniors dedicate 20e45 minutes
for each resistance training session.
3.1.5. Rest periods and physical environments
Longer rest periods between exercise sessions as well as safe physical environments are imperative for seniors[34].
3.1.6. Breathing
Seniors should not hold their breath during resistance training. Lifting belts and abdominal strengthening exercise may be used to help stabilize the torso in order to facilitate breathing[35].
3.1.7. Active muscles
Exercise programs that target knee and hip extension and flexion should both be performed on a regular basis [35]. Antagonistic muscles should also be exercised to keep bal-ance. ACMS[36]recommends including all six major muscle groups (chest, shoulders, arms, back, abdomen and legs) into a comprehensive resistance training programs.
Several studies have elucidated additional details of an optimal resistance training program. Taaffe[33]suggests that 8e12 repetitions should be performed per set. When the in-dividual is able to perform 12 repetitions, the resistance should be increased to a point where only 8 repetitions are possible. A minimum of one set, but preferably 2e3 sets, per exercise session is appropriate with 1e2 minutes of rest be-tween each set. The author also recommends exercising 1e3 days per week, for no more than one hour per session and with at least 48 hours between sessions.
3.2. Implications and application into daily clinical practice
Physical frailty in the elderly, especially the impairment in lower extremity strength, has been widely described in the geriatric literature as declining physiological conditions and has been used to screen and identify high-risk individuals for adverse health events [37]. Physical frailty has also been recognized as an indicator for fall events in the elderly. The significant impact of falls has been well-documented. The elderly who fall increase healthcare costs and patients/family members may also experience emotional challenges. There-fore, physical frailty needs to be addressed to prevent or minimize the occurrence of falls in the elderly.
Sarcopenia in the lower extremities has long been recog-nized as a contributing factor to physical frailty. Many studies have found an association between physical frailty and sar-copenia. In fact, sarcopenia and physical frailty have been regarded as two sides of the same coin[38]. They can overlap and contribute to physical function impairment, such as slow gait speed or poor balance. Sarcopenia and physical frailty can also affect each other, greatly impacting critical physiological parameters. Recent studies conducted in elderly trauma pa-tients further confirmed that sarcopenia and frailty work hand-in-hand in critical discharge disposition parameters, e.g. skilled-nursing facility, nursing home, rehabilitation, home and home health[39].
Therefore, seniors should perform progressive resistance exercise training to delay or prevent the development of physical frailty and its significant negative health conse-quences. Clinicians can adopt the guidelines from ACMS to design elderly-tailored progressive and rigorous resistance training programs to delay sarcopenia and therefore improve the quality of life for seniors.
4.
Conclusion
Sarcopenia, the loss of muscle mass and strength, has a crucial negative impact on seniors' physical functioning, in-dependence and quality of life. Some biological and lifestyle factors that occur during aging, such as the decreased number of motor units, lower mixed protein synthesis rates and al-terations in circulating hormones, contribute to the occur-rence of sarcopenia among the elderly. Progressive resistance training involving major muscles is a simple and effective way to counteract sarcopenia.
Some important implications for clinical elder care can be drawn from this review. First of all, geriatric care staff should be knowledgeable about sarcopenia and its tremendously detrimental effects. Strategies should be implemented in a timely manner to delay the process of sarcopenia or to prevent severe negative outcomes. Secondly, as resistance training plays a significant role in sarcopenia management, seniors are strongly encourage to encourage in moderate resistance ex-ercise, or at least keep physically active. It is vital for geriatric professionals to follow exercise guidelines when advising exercise modalities in order to maximize the exercise benefits and effectively address the severe outcomes of sarcopenia.
r e f e r e n c e s
[1] Ortman J, Velkoff V, Hogan H. An aging nation: the older population in the United States. Population estimates and Projections. Curr Popul reports [Internet]. U.S. Department of Commerce. Economics and Statistics Administration. U. S Census Bur; 2014 May [cited 2015 Jan 6]. Available from:,
http://www.census.gov/prod/2014pubs/p25-1140.pdf. [2] Schneider EL, Guralnik JM. The aging of America. Impact on
health care costs. JAMA 1990;263(17):2335e40.
[3] Deschenes MR. Effects of aging on muscle fibre type and size. Sports Med 2004;34(12):809e24.
[4] Epidemiologic and methodologic problems in determining nutritional status of older persons. In: Proceedings of a
conference. Albuquerque: New Mexico; October 19-21, 1988. p. 1121e235. Am J Clin Nutr 1989;50(5 Suppl).
[5] Rolland Y, Czerwinski S, van Kan G, Morley JE, Cesari M, Onder G, et al. Sarcopenia: Its assessment, etiology, pathogenesis, consequences and future perspectives. J Nutr Health Aging 2008;12(7):433e50.
[6] Cruz-Jentoft AJ, Landi F, Topinkova E, Michel JP. Understanding sarcopenia as a geriatric syndrome. Curr Opin Clin Nutr Metab Care 2010;13(1):1e7.
[7] Baumgartner RN, Koehler KM, Gallagher D, Romero L, Heymsfield SB, Ross RR, et al. Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol 1998;147(8):755e63.
[8] Forbes GB, Reina JC. Adult lean body mass declines with age: some longitudinal observations. Metabolism
1970;19(9):653e63.
[9] Roubenoff R. Sarcopenia and its implications for the elderly. Eur J Clin Nutr 2000;54(suppl. 3):S40e7.
[10] Kamel HK. Sarcopenia and aging. Nutr Rev 2003;61(5Pt1):157e67.
[11] Murphy RA, Ip EH, Zhang Q, Boudreau RM, Cawthon PM, Newman AB, et al. Transition to sarcopenia and
determinants of transitions in older adults: a population-based study. J Gerontol A Biol Sci Med Sci 2014;69(6):751e8. [12] Szulc P, Beck TJ, Marchand F, Delmas PD. Low skeletal
muscle mass is associated with poor structural parameters of bone and impaired balance in elderly men - the MINOS study. J Bone Min Res 2005;20(5):721e9.
[13] Metter EJ, Talbot LA, Schrager M, Conwit R. Skeletal muscle strength as a predictor of all-cause mortality in healthy men. J Gerontol A Biol Sci Med Sci 2002;57(10):B359e65.
[14] Kritz-Silverstein D, Barrett-Connor E. Grip Strength and Bone Mineral Density in older women. J Bone Min Res 1994;9(1):45e51. [15] Katz LD, Glickman MG, Rapoport S, Ferrannini E,
DeFronzo RA. Splanchnic and peripheral disposal of oral glucose in man. Diabetes 1983;32(7):675e9.
[16] Yuan H, Goto N, Akita H, Shiraishi N, He HJ. Morphometric analysis of the human cervical motoneurons in the aging process. Okajimas Folia Anat Jpn 2000;77(1):1e4.
[17] McNeil CJ, Doherty TJ, Stashuk DW, Rice CL. Motor unit number estimates in the tibialis anterior muscle of young, old, and very old men. Muscle Nerve 2005;31(4):461e7. [18] Sperling L. Evaluation of upper extremity function in
70-year-old men and women. Scand J Rehabil Med 1980;12(4):139e44. [19] Balagopal P, Rooyackers OE, Adey DB, Ades PA, Nair KS.
Effects of aging on in vivo synthesis of skeletal muscle myosin heavy-chain and sarcoplasmic protein in humans. Am J Physiol 1997;273(4Pt1):E790e800.
[20] Balagopal P, Schimke JC, Ades P, Adey D, Nair KS. Age effect on transcript levels and synthesis rate of muscle MHC and response to resistance exercise. Am J Physiol Endocrinol Metab 2001;280(2):E203e8.
[21] Greenlund LJ, Nair KS. Sarcopeniadconsequences, mechanisms, and potential therapies. Mech Ageing Dev 2003;124(3):287e99.
[22] van den Beld AW, de Jong FH, Grobbee DE, Pols HA, Lamberts SW. Measures of bioavailable serum testosterone and estradiol and their relationships with muscle strength, bone density, and body composition in elderly men. J Clin Endocrinol Metab 2000;85(9):3276e82.
[23] Bhasin S, Tenover JS. Age-associated sarcopeniaeissues in the use of testosterone as an anabolic agent in older men. J Clin Endocrinol Metab 1997;82(6):1659e60.
[24] Gooren L. Endocrine aspects of ageing in the male. Mol Cell Endocrinol 1998;145(1e2):153e9.
[25] Veldhuis JD, Iranmanesh A, Weltman A. Elements in the pathophysiology of diminished growth hormone (GH) secretion in aging humans. Endocrine 1997;7(1):41e8.
[26] Wells S. Growth hormone and insulin-like growth factor-I as anabolic agents. Curr Opin Clin Nutr Metab Care
1998;1(3):257e62.
[27] Bales CW, Ritchie CS. Sarcopenia, weight loss, and nutritional frailty in the elderly. Annu Rev Nutr 2002;22:309e23.
[28] Morgan KT. Nutrition, resistance training, and sarcopenia: their role in successful aging. Top Clin Nutr
2012;27(2):114e23.
[29] Yarasheski KE, Pak-Loduca J, Hasten DL, Obert KA, Brown MB, Sinacore DR. Resistance exercise training increases mixed muscle protein synthesis rate in frail women and men 76 yr old. Am J Physiol
1999;277(1Pt1):E118e25.
[30] Fiatarone MA, O'Neill EF, Ryan ND, Clements KM, Solares GR, Nelson ME, et al. Exercise training and nutritional
supplementation for physical frailty in very elderly people. N Engl J Med 1994;330(25):1769e75.
[31] Frontera WR, Meredith CN, O'Reilly KP, Knuttgen HG, Evans WJ. Strength conditioning in older men: skeletal muscle hyperthrophy and improved function. J Appl Physiol 1988;64(3):1038e44.
[32] Fry CS, Drummond MJ, Glynn EL, Dickinson JM,
Gundermann DM, Timmerman KL, et al. Skeletal muscle autophagy and protein breakdown following resistance
exercise are similar in younger and older adults. J Gerontol A Biol Sci Med Sci 2013;68(5):599e607.
[33] Taaffe DR. SarcopeniaeExercise as a treatment strategy. Aust Fam Physician 2006;35(3):130e4.
[34] Nayak N, Randall K, Shankar K. Exercise in the elderly. Philadelphia: Hanley&Belfus; 1999.
[35] Power S, Howley E. Exercise physiology: theory and application to fitness and performance. 8th ed. New York: McGraw-Hill Humanities/Social Sciences/Languages; 2011. [36] Willoughby D. Resistance training and the older adult.
[homepage Internet]. No date [cited 2015 Jan 15]. Available from:https://www.acsm.org/docs/current-comments/ resistancetrainingandtheoa.pdf.
[37] Fielding RA, Vellas B, Evans WJ, Bhasin S, Morley JE, Newman AB, et al. Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. International working group on sarcopenia. J Am Med Dir Assoc 2011;12(4):249e56.
[38] Cesari M, Landi F, Vellas B, Bernabei R, Marzetti E. Sarcopenia and physical frailty: two sides of the same coin. Front Aging Neurosci 2014;6:192.
[39] Fairchild B, Webb TP, Xiang Q, Tarima S, Brasel KJ. Sarcopenia and frailty in elderly trauma patients. World J Surg 2015;39(2):373e9.