Aging Skeletal Muscle: Physiologic Changes and the Effects of Training Glenn N Williams, Michael J Higgins and Michael

D Lewek PHYS THER. 2002; 82:62-68.

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Update

Aging Skeletal Muscle: Physiologic Changes and the Effects of Training

ccording to the 1996 US Census Bureau population projections (middle series), during the period from 1995 through 2030, the percentage of the American population that is 65 years of age or older and 85 years of age or older will increase by 107% and 133%, respectively. In contrast, the percentage of those under 65 years of age will increase by only 21%.1 In addition, the percentages of older people with disabilities in activities of daily living and of older people requiring institutionalization for disabilities are expected to remain similar to current levels over the next 30 years, although these statistics vary by ethnicity.1 This means that the number of people requiring institutionalization for disabilities will increase substantially. Based on these data, the physiologic changes that occur in skeletal muscle as a result of aging and the effects of exercise on aging skeletal muscle are going to be of increased importance to physical therapists. The purpose of this update is to discuss the effects of aging on skeletal muscle and to discuss how exercise affects aging skeletal muscle. Effect of Aging on Skeletal Muscle As humans age, the force-generating capacity (strength) of their skeletal muscles is reduced.2,3 As a result, many older people experience difficulty in performing their activities of daily living.2 Recent research indicates that the observed loss of force production in older people is primarily to the result of muscle atrophy and alterations in the percentage of contractile tissue within muscle3 6 rather than deficits in muscle activation (motor unit [MU] recruitment and firing rates).79

APTA is a sponsor of the Decade, an international, multidisciplinary initiative to improve health-related quality of life for people with musculoskeletal disorders.

[Williams GN, Higgins MJ, Lewek MD. Aging skeletal muscle: physiologic changes and the effects of training. Phys Ther. 2002;82:62 68.]

Key Words: Aging, Exercise, Muscle, Skeletal muscle, Training. Glenn N Williams, Michael J Higgins, Michael D Lewek

62

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A common misconception is
Effects on Muscle Fiber Number and Size Skeletal muscle cross-sectional area (CSA) decreases with age (Fig. 1).3,4,6 This phenomenon, which is referred to as sarcopenia, can be the result of a reduction in fiber size, fiber number, or a combination of the two. Most researchers who have investigated sarcopenia have used either imaging techniques or muscle biopsies that have been performed in a cross-sectional manner.10 14 Frontera et al,3 however, reported no changes in the fiber size of the vastus lateralis muscles of sedentary men without impairments, aged 60 to 70 years at the beginning of the study, who underwent muscle biopsies in 19851986 and then again 12 years later. Because studies that depend on muscle biopsies have some inherent shortcomings (eg, being confined to a limited region of a muscle), many researchers consider whole muscle sampling to be the gold standard for analyzing muscle fiber size and number. The results of microscopic evaluation of cross-sections from whole human vastus lateralis muscles suggest that, although a small reduction in fiber size may occur, a reduction in the total number of fibers within a muscle is the primary source of sarcopenia (Fig. 1).4 Researchers have also demonstrated that, in addition to the decrease in skeletal muscle CSA, the muscles of older people (65 83 years of age) contain less contractile tissue and more noncontractile tissue when compared with the skeletal muscle of younger people (26 44 years of age).6 A greater per-

that older people need to take it easy when performing exercise.

centage of noncontractile tissue (fat and connective tissue) results in a decreased force production capability. The change in tissue composition in older people suggests that their muscle mass may be reduced to a greater extent than can be determined by measurements of muscle CSA alone. Researchers examining the cause of skeletal muscle atrophy in older people have often focused on how age affects the fiber types of muscle.2,4,13 In recent reviews of aging and muscle morphology, some authors2,15 have concluded that the size of type I (slow) fibers does not change substantially with age, but that type II (fast) fibers undergo selective atrophy (Fig. 2). Although the general consensus is that only type II fibers are greatly reduced in size with aging (in people without impairments), the number of type I and type II fibers appears

GN Williams, PT, SCS, is a doctoral student in the Biomechanics and Movement Science Program at the University of Delaware, Department of Physical Therapy, 301 McKinly Laboratory, Newark, DE 19716 (USA) (glennwms@udel.edu). Address all correspondence to Mr Williams. MJ Higgins, PT, MEd, ATC, is Assistant Professor and Athletic Trainer, Department of Health and Exercise Sciences, and a doctoral student in the Biomechanics and Movement Science Program at the University of Delaware. MD Lewek, PT, is a doctoral student in the Biomechanics and Movement Science Program at the University of Delaware. All authors provided concept/research design and writing. The authors acknowledge Dr Stuart Binder-Macleod, Scott Stackhouse, Darcy Reisman, Jennifer Stevens, and Wayne Scott for their consultation and review of the manuscript. Mr Williams is supported, in part, by the Foundation for Physical Therapy; Mr Lewek is supported by NIH training grant T32 HD07490.

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Williams et al . 63

orphaned muscle fibers are often reinnervated by one of the existing MUs through collateral sprouting.21 Therefore, although there is a reduction in the number of MUs, some MUs become larger.21 In addition to these changes in MU morphology, some researchers7,22,23 have demonstrated that MU firing rates are altered with aging. Some researchers have indicated that MU firing rates decrease with age,7,22 whereas others have indicated that MU firing rates do not decrease,9,23 but may become more variable.23 Some authors21 have attributed this variability in the MU firing rates of older people Figure 1. The relationship between age and (A) muscle cross-sectional area and (B) the total number of to a preferential denervation of type II muscle fibers. Reproduced with permission of Elsevier Science from Lexell J, Taylor CC, Sjostrom fibers and a subsequent reinnervation M. What is the cause of the ageing atrophy? Total number, size, and proportion of different through collateral sprouting by neighfiber types studied in whole vastus lateralis muscle from 15- to 83-year-old men. J Neurol Sci. boring MUs normally associated with 1988;84:275294. type I fibers. Increased variability in MU firing rates may lead to deficiencies in motor control and force production. The reinnervation of denervated type II muscle fibers by neighboring type I MUs has also been implicated in the increased co-expression of type I and type II myosin heavy chain (MHC) isoforms observed in the skeletal muscle of older individuals.21,24 Myosin heavy chains are the head portions of the myosin molecule that determine the rate of cross-bridge reactions with actin filaments and, consequently, the speed of muscle contraction. In a recent study where researchers analyzed the vastus lateralis muscles of very old people (mean age88 years), the muscles of these participants had greater Figure 2. The effect of aging on (A) type I fiber, type II fiber, and mean fiber size, and (B) the proportion co-expression of MHC isoforms than of type I fibers in human vastus lateralis muscle. Reproduced with permission of Elsevier Science was observed in younger subjects.24 The from Lexell J, Taylor CC, Sjostrom M. What is the cause of the ageing atrophy? Total number, researchers attributed this increased size, and proportion of different fiber types studied in whole vastus lateralis muscle from 15- to co-expression of MHC isoforms to mus83-year-old men. J Neurol Sci. 1988;84:275294. cle fibers co-expressing both the isoforms of the denervated parent MUs to decline in a similar manner with age.2 Contrary to the and the isoforms of the MUs that reinnervated these general belief that the percentage of type I fibers fibers.24 2,4 remains unchanged with aging (Fig. 2), one research group suggests that it decreases; however, the authors Andersen et al24 also attributed the increased warn that, because of methodological concerns, their co-expression of MHC isoforms in older people to an results should be interpreted with caution until further alteration or malfunction in protein synthesis.24 More3 evidence exists. over, declines in protein synthesis rates have led to decreases in muscle mass, which is determined by the Effects on Motor Unit Characteristics ratio between protein synthesis and breakdown.25 Because the number of -motoneurons decreases with Research indicates that the aggregate synthesis rate for age,16 19 older people have fewer MUs10,20; however, muscle proteins (eg, myofibrillar, mitochondrial, and

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Table.
A Sample Progressive Resistance Training Program Period of Training Weeks 13 Weeks 48 Weeks 912
a

mass, decreased force production, and increased MHC co-expression.2,27,29,30,3336 Skeletal muscle adaptations in response to strength training occur in older people, and researchers have studied this phenomenon primarily using 1 of 2 types of training: (1) progressive resistance training (PRT) programs33,34 or (2) high-intensity training programs.3538 An example of a PRT program is provided in the Table. High-intensity resistance programs usually consist of 2 to 6 sets of 8 repetitions at approximately 80% of a persons one-repetition maximum (1-RM).28,35,38 Although subjects in these studies have generally trained 3 times per week,34,35,39,40 one research group reported that resistance training (3 sets of 8 exercises at 80% of the subjects 1-RM) performed once or twice weekly resulted in similar gains in force production as the same program performed 3 times per week.37 A common misconception is that older people need to take it easy when performing exercise. Although this may be true when initiating an exercise program or in the presence of comorbidities (eg, heart disease, diabetes, balance disorders), some researchers suggest that older people who are healthy respond to strength and endurance training in a similar fashion to younger people.2,28,41 Many physical therapists, therefore, may not be training their older patients at intensities that are optimally suited to induce the desired training effects. Effect on Oxidative Capacity and Muscle Capillarization Muscle capillarization and oxidative capacity are 2 measures of skeletal muscle adaptation to training (both endurance and strength training). In the skeletal muscle of older people, both the muscle fiber-to-capillary ratio and oxidative capacity are often decreased when compared with the skeletal muscle of younger people.13 According to Coggan and colleagues,27 muscle capillarization increased in older individuals (60 70 years of age) who engaged in an endurance training program that consisted of walking or jogging for 45 minutes per day, 3 times per week, for 10 months at 80% of their age-adjusted maximal heart rate (exercise stimulus was progressively increased over the period of study as the participants adapted to training). More specifically, the capillary densities (capillaries per square millimeter) of these participants increased by 20%, whereas the number of capillaries per muscle fiber increased by 25%.27 These findings imply that new capillaries were generated in the muscle. Meredith et al42 studied the peripheral effects of endurance training on 65-year-old men who performed cycle ergometry at 70% of their age-adjusted maximal heart rate for 45 minutes per day, 3 days per week. In their study, they demonstrated that the oxidative capacity of

No. of Repetitions 3 sets of 815 3 sets of 810 3 sets of 46

Training Intensity 50%60% of 1-RMa 60%75% of 1-RM 75%90% of 1-RM

1-RMone-repetition maximum.

sarcoplasmic) declines with age, although not all muscle proteins demonstrate altered synthesis rates with aging.25 Separation of these proteins has revealed that MHC synthesis rates are reduced in people who are of middle age (521 years) and old age (772 years) and that protein synthesis rates correlate well with reductions in muscle mass and muscle force production per unit of muscle mass.25 In addition to reduced muscle mass, Delbono et al26 also attributed decreased muscle force production to alterations in intrinsic muscle function in aged people. Because muscle force production is often reduced to a greater extent than muscle mass in older people,2 the mechanisms by which the muscles of older people produce force is currently a topic of interest among muscle physiologists. At the cellular level, alterations in the sarcoplasmic reticulum (SR) have been hypothesized to be responsible for reduced muscle force.25 Delbono and colleagues26 have reported that the amount of SR Ca 2 released in response to sarcolemmal depolarization is reduced in aged skeletal muscle. Because research has demonstrated that adequate Ca 2 is available for release, these authors have suggested that an uncoupling between sarcolemmal excitation and the release of Ca 2 by the SR (excitation-contraction uncoupling) results in diminished skeletal muscle force production in older people.26 Reduced muscle mass alone does not appear to fully explain the deficits in force production observed in older people (60 years of age). Effects of Training Training of muscle is typically divided into 2 major categories: endurance and strength training. Endurance training refers to exercise directed at improving stamina (the duration that a person can maintain strenuous o2max), whereas strength activity) and aerobic capacity (V training refers to exercise directed at improving the maximum force-generating capacity of muscle. There is evidence that training has a positive effect on aging skeletal muscle.2,2730 Training-induced adaptations in skeletal muscle depend on the intensity, frequency, duration, and mode of exercise.30 32 Appropriate exercise can alter, slow, or even partially reverse some of the age-related physiological changes that occur in skeletal muscle, including sarcopenia, reduced lean muscle

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Older people (aged 60 97 years) who perform regular resistance training have been shown to have increases in force production and muscle fiber CSA (Fig. 3).33,34,43 Hakkinen et al33 studied quadriceps femoris muscle force production and fiber characteristics of older people (mean age [SD]723 years and 673 years for men and women, respectively) who performed a 6-month training program consisting of progressive heavy resistance and explosive strength Figure 3. training. The participants in this The effects of high-intensity strength training on older peoples (A) knee extensor (top line) and research performed 2 lower-extremity flexor (bottom line) muscle force, and (B) type I fiber, type II fiber, and mean fiber cross-sectional exercisesthe bilateral leg press and areas (MFA). Results are meanstandard error. Asterisk indicates significantly different from pretraining measurements (P .05). Reprinted with permission of the American Physiological the knee extension exercise. ParticiSociety from Frontera WR, Meredith CN, OReilly KP, et al. Strength conditioning in older men: pants extended their knees as exploskeletal muscle hypertrophy and improved function. J Appl Physiol. 1988;64:1038 1044. sively as possible against light loads during 20% of the knee extension exercise repetitions, whereas they performed the rest of the repetitions in a slow and conthe older mens muscles increased by 125%.42 In additrolled fashion. During the first 2 months of training, tion, Frontera and colleagues35 found that a highparticipants exercised twice per week with loads of 50% intensity strength training program increased particito 70% of their 1-RM, and they performed 3 to 4 sets of pants capillary per muscle fiber ratio by 15%. The 10 to 15 repetitions of both exercises. During the third strength training program used in this research conand fourth months, the participants performed 8 to 12 sisted of 34 training sessions performed at a frequency of explosive repetitions and 3 to 5 sets of 5 to 6 repeti3 times per week (a 12-week program with 2 sessions tions with 60% to 80% of their 1-RM for the controlled used for testing) in which participants performed 3 sets repetitions. The frequency of training during this period of 8 repetitions of knee extension and knee flexion was twice per week. During the last 2 months of training, exercises at 80% of their 1-RM. Participants 1-RM was the participants also performed 8 to 12 repetitions of assessed and adjusted at the end of each week. These explosive knee extensions with 50% to 60% of their results indicate that training can have a profound effect 1-RM and then performed 4 to 6 sets of 3 to 6 repetitions on the oxidative capacity of an elderly persons skeletal muscle. with 70% to 80% of their 1-RM for the remaining exercise. The frequency was again twice per week. The Effects on Muscle Fiber Characteristics participants 1-RM was reassessed and adjusted every Researchers14,27,33,34 have suggested that both endurance second month during this research. Testing performed and strength training can limit the extent of sarcopenia at the end of the 6-month program demonstrated that in elderly people. Coggan and colleagues27 reported the force production of the quadriceps femoris muscles that, after 10 months of endurance training that conin these participants increased by 30% to 60%, although sisted of walking or jogging for 45 minutes per day, 3 their CSA increased to a lesser degree.33 times per week, the type I (slow) fiber CSA of the lateral gastrocnemius muscles of 60- to 70-year-old participants Harridge et al34 enrolled participants who were very old increased by 12% in both male and female participants, (age8597 years) in a quadriceps femoris muscle trainthe type IIA fiber (fast, fatigue-resistant) CSA increased ing program in which participants performed progresby 6% in male participants and by 18% in female sive resistive training 3 times per week for 12 weeks. participants, and the type IIB fiber (fast, fatigable) CSA During the first week of training, the participants perincreased by 12% in male participants and by 9% in formed 3 sets of 8 knee extensions with a load of 50% of female participants. These researchers also indicated their 1-RM. During weeks 2 through 12, the participants that, although the percentage of type I fibers remained performed 3 sets of knee extensions with a load of 80% unchanged after endurance training, there was a of their 1-RM. The participants 1-RM was reassessed and decrease in the percentage of type IIB fibers and an 8% adjusted every 2 weeks. After 3 months of training, the increase in the percentage of type IIA fibers (implying a participants quadriceps femoris muscle force producconversion of type IIB fibers to type IIA with training).27 tion had increased by an average of 134%, whereas their lean CSA (contractile tissue only) had increased by

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10%.34 Other researchers have also reported force gains (48%-174%) with associated moderate gains in CSA (15%-17%) with similar training programs.36,38 In these studies, researchers demonstrated that high-intensity training can have an effect on muscle force and CSA in older people and suggested that the deleterious effects of aging on skeletal muscle can be reduced with training. Effects on Motor Unit Characteristics Several researchers33,34,36,38 have demonstrated that, although gains in both CSA and force production occur with training, the observed gains in force are generally much greater than the gains observed in muscle CSA. This finding is understandable because increases in force production occur not only from increases in skeletal muscle CSA (hypertrophy), but also as a result of training-related neural adaptations (eg, changes in the recruitment and firing rates of MUs).14,33 Neural adaptations have been reported to be the primary source of force production gains observed in the first 8 weeks of training, whereas increases in muscle CSA are believed to be the primary source of the force production gains observed thereafter.28 Most research on the effects of training on older people has been conducted with relatively untrained participants doing high-intensity training. For this reason, it is likely that training-related neural adaptations were responsible for a notable portion of the gains in force production observed in these studies. Secondary Effects Related to Training and Skeletal Muscle Researchers suggest that the skeletal muscle of older people are damaged more easily with the loading that occurs during training when compared with the skeletal muscle of younger people.35,44 47 As a result, older patients may be more susceptible to muscle injuries and soreness after exercise than younger patients.45 47 There is also some evidence that indicates that older people who regularly train may have higher dietary protein requirements than younger people who perform similar exercise.44 Consequently, a dietary protein supplement, in theory, may be useful in promoting optimal muscle growth in older people who are doing strength training exercise. Osteoporosis is a common health disorder in older people. Several researchers have investigated the relationship between skeletal muscle mass and bone mineral density (BMD).48 52 Although not all researchers have demonstrated a relationship between skeletal muscle mass and BMD, there is a large body of evidence that suggests that osteoporosis and sarcopenia are related.48,49,52 Some authors48 53 believe that aerobic exercises that load the lower extremities substantially (eg, running) and strength training help to prevent or slow osteopo-

rosis because of the observed relationship between sarcopenia and BMD as well as the effects of weight bearing on bone. Muscle contractions during strength training repetitively load bone. Researchers48,49,52 suggest that the repetitive loading that occurs with strength training can maintain or increase BMD. Some research has even indicated that strength training may result in fewer fractures in elderly people because of its effect on BMD.48,52 Summary Changes occur in skeletal muscle with aging. The most apparent changes are decreases in muscle CSA and the volume of contractile tissue within that CSA. Changes also occur in the function of muscle fibers, in MU firing characteristics, and in the aerobic capacity of skeletal muscle. The results of these changes are decreased force production and often decreased function. There is evidence that exercise can have an impact on the size, strength, and aerobic capacity of skeletal muscle in older people. Research suggests that regular exercise including strength and endurance training of adequate intensity can reduce some of the physiologic effects of aging seen in skeletal muscle.
References
1 Siegal J. Aging Into the 21st Century. Washington, DC: Dept of Health and Human Services, Administration on Aging, National Aging Information Center; May 31, 1996. NAIC-30. 2 Rogers MA, Evans WJ. Changes in skeletal muscle with aging: effects of exercise training. Exerc Sport Sci Rev. 1993;21:65102. 3 Frontera WR, Hughes VA, Fielding RA, et al. Aging of skeletal muscle: a 12-yr longitudinal study. J Appl Physiol. 2000;88:13211326. 4 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. 1988;84:275294. 5 Lexell J, Taylor CC. Variability in muscle fibre areas in whole human quadriceps muscle: effects of increasing age. J Anat. 1991;174:239 249. 6 Kent-Braun JA, Ng AV, Young K. Skeletal muscle contractile and noncontractile components in young and older women and men. J Appl Physiol. 2000;88:662 668. 7 Connelly DM, Rice CL, Roos MR, Vandervoort AA. Motor unit firing rates and contractile properties in tibialis anterior of young and old men. J Appl Physiol. 1999;87:843 852. 8 Kent-Braun JA, Ng AV. Specific strength and voluntary muscle activation in young and elderly women and men. J Appl Physiol. 1999;87:2229. 9 Roos MR, Rice CL, Connelly DM, Vandervoort AA. Quadriceps muscle strength, contractile properties, and motor unit firing rates in young and old men. Muscle Nerve. 1999;22:1094 1103. 10 Vandervoort AA, McComas AJ. Contractile changes in opposing muscles of the human ankle joint with aging. J Appl Physiol. 1986;61: 361367. 11 Young A, Stokes M, Crowe M. Size and strength of the quadriceps muscles of old and young women. Eur J Clin Invest. 1984;14:282287.

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12 Young A, Stokes M, Crowe M. The size and strength of the quadriceps muscles of old and young men. Clin Physiol. 1985;5:145154. 13 Coggan AR, Spina RJ, King DS, et al. Histochemical and enzymatic comparison of the gastrocnemius muscle of young and elderly men and women. J Gerontol. 1992;47:B71B76. 14 Hakkinen K, Kraemer WJ, Kallinen M, et al. Bilateral and unilateral neuromuscular function and muscle cross-sectional area in middleaged and elderly men and women. J Gerontol A Biol Sci Med Sci. 1996;51:B21B29. 15 Porter MM, Vandervoort AA, Lexell J. Aging of human muscle: structure, function, and adaptability. Scand J Med Sci Sports. 1995;5: 129 142. 16 Gardner E. Decrease in human neurones with age. Anatomical Record. 1940;77:529 536. 17 Tomlinson BE, Irving D. The numbers of limb motor neurons in the human lumbosacral cord throughout life. J Neurol Sci. 1977;34:213219. 18 Kawamura Y, Okazaki H, OBrien PC, Dych PJ. Lumbar motoneurons of man, I: number and diameter histogram of alpha and gamma axons of ventral root. J Neuropathol Exp Neurol. 1977;36:853 860. 19 Mittal KR, Logmani FH. Age-related reduction in 8th cervical ventral nerve root myelinated fiber diameters and numbers in man. J Gerontol. 1987;42:8 10. 20 Campbell MJ, McComas AJ, Petito F. Physiological changes in ageing muscles. J Neurol Neurosurg Psychiatry. 1973;36:174 182. 21 Roos MR, Rice CL, Vandervoort AA. Age-related changes in motor unit function. Muscle Nerve. 1997;20:679 690. 22 Erim Z, Beg MF, Burke DT, de Luca CJ. Effects of aging on motor-unit control properties. J Neurophysiol. 1999;82:20812091. 23 Laidlaw DH, Bilodeau M, Enoka RM. Steadiness is reduced and motor unit discharge is more variable in old adults. Muscle Nerve. 2000;23:600 612. 24 Andersen JL, Terzis G, Kryger A. Increase in the degree of coexpression of myosin heavy chain isoforms in skeletal muscle fibers of the very old. Muscle Nerve. 1999;22:449 454. 25 Balagopal P, Rooyackers OE, Adey DB, et al. Effects of aging on in vivo synthesis of skeletal muscle myosin heavy-chain and sarcoplasmic protein in humans. Am J Physiol. 1997;273:E790 E800. 26 Delbono O, Renganathan M, Messi ML. Excitation-Ca releasecontraction coupling in single aged human skeletal muscle fiber. Muscle Nerve Suppl. 1997;5:S88 S92. 27 Coggan AR, Spina RJ, King DS, et al. Skeletal muscle adaptations to endurance training in 60- to 70-yr-old men and women. J Appl Physiol. 1992;72:1780 1786. 28 Kraemer WJ, Fleck SJ, Evans WJ. Strength and power training: physiological mechanisms of adaptation. Exerc Sport Sci Rev. 1996;24: 363397. 29 Hurley BF, Hagberg JM. Optimizing health in older persons: aerobic or strength training? Exerc Sport Sci Rev. 1998;26:61 89. 30 Adams K, OShea P, OShea K. Aging: its effects on strength, power, flexibility, and bone density. Natl Strength Assoc Cond J. 1999;21:6577. 31 Fleck SJ, Kraemer WJ. Designing Resistance Training Programs. Champaign, Ill: Human Kinetics; 1987. 32 Pearson D, Massetti S. Periodization at a glance. Natl Strength Cond Assoc J. 1999;21:5253. 33 Hakkinen K, Kallinen M, Izquierdo M, et al. Changes in agonistantagonist EMG, muscle CSA, and force during strength training in middle-aged and older people. J Appl Physiol. 1998;84:13411349.
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Aging Skeletal Muscle: Physiologic Changes and the Effects of Training Glenn N Williams, Michael J Higgins and Michael D Lewek PHYS THER. 2002; 82:62-68.

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