Aging skeletal muscle: physiologic changes and the effects of training. (Update).

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 1985-1986 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 percentage 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.

[FIGURE 1 OMITTED]

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 authors (2,15) 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 to decline in a similar manner with age. (2) Contrary to the general belief that the percentage of type I fibers remains unchanged with aging (Fig. 2), (2,4) one research group suggests that it decreases; however, the authors warn that, because of methodological concerns, their results should be interpreted with caution until further evidence exists. (3)

[FIGURE 2 OMITTED]

Effects on Motor Unit Characteristics

Because the number of [alpha]-motoneurons decreases with age, (16-19) older people have fewer Ums (10,20); however, "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 researchers (7,22,23) 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 authors (21) have attributed this variability in the MU firing rates of older people to a preferential denervation of type II fibers and a subsequent reinnervation through collateral sprouting by neighboring MUs normally associated with 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 age = 88 years), the muscles of these participants had greater co-expression of MHC isoforms than was observed in younger subjects. (24) The researchers attributed this increased co-expression of MHC isoforms to muscle fibers co-expressing both the isoforms of the denervated parent MUs and the isoforms of the MUs that reinnervated these fibers. (24)

Andersen et al (24) also attributed the increased co-expression of MHC isoforms in older people to an alteration or malfunction in protein synthesis. (24) Moreover, declines in protein synthesis rates have led to decreases in muscle mass, which is determined by the ratio between protein synthesis and breakdown. (25) Research indicates that the aggregate synthesis rate for muscle proteins (eg, myofibrillar, mitochondrial, and 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 (52 [+ or -] 1 years) and old age (77 [+ or -] 2 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 al (26) 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 colleagues (26) have reported that the amount of SR [Ca.sup.2+] released in response to sarcolemmal depolarization is reduced in aged skeletal muscle. Because research has demonstrated that adequate [Ca.sup.2+] is available for release, these authors have suggested that an uncoupling between sarcolemmal excitation and the release of [Ca.sup.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 ([greater than or equal to] 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 activity) and aerobic capacity ([Vo.sub.2]max), whereas strength 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. (2,27-30) 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 mass, decreased force production, and increased MHC co-expression. (2,27,29,30,33-36)

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) programs (33,34) or (2) high-intensity training programs. (35-38) 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 person's 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 subject's 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 al (42) 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 the older men's muscles increased by 125%. (42) In addition, Frontera and colleagues (35) found that a high-intensity strength training program increased participants' capillary per muscle fiber ratio by 15%. The strength training program used in this research consisted of 34 training sessions performed at a frequency of 3 times per week (a 12-week program with 2 sessions used for testing) in which participants performed 3 sets of 8 repetitions of knee extension and knee flexion exercises at 80% of their 1-RM. Participants' 1-RM was assessed and adjusted at the end of each week. These results indicate that training can have a profound effect on the oxidative capacity of an elderly person's skeletal muscle.

Effects on Muscle Fiber Characteristics

Researchers (14,27,33,34) have suggested that both endurance and strength training can limit the extent of sarcopenia in elderly people. Coggan and colleagues (27) reported that, after 10 months of endurance training that consisted of walking or jogging for 45 minutes per day, 3 times per week, the type I (slow) fiber CSA of the lateral gastrocnemius muscles of 60- to 70-year-old participants increased by 12% in both male and female participants, the type IIA fiber (fast, fatigue-resistant) CSA increased by 6% in male participants and by 18% in female participants, and the type IIB fiber (fast, fatigable) CSA increased by 12% in male participants and by 9% in female participants. These researchers also indicated that, although the percentage of type I fibers remained unchanged after endurance training, there was a decrease in the percentage of type IIB fibers and an 8% increase in the percentage of type IIA fibers (implying a conversion of type IIB fibers to type IIA with training). (27)

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 al (33) studied quadriceps femoris muscle force production and fiber characteristics of older people (mean age [[+ or -] SD] = 72 [+ or -] 3 years and 67 [+ or -] 3 years for men and women, respectively) who performed a 6-month training program consisting of progressive heavy resistance and "explosive" strength training. The participants in this research performed 2 lower-extremity exercises--the bilateral leg press and the knee extension exercise. Participants extended their knees as "explosively" 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 controlled fashion. During the first 2 months of training, participants exercised twice per week with loads of 50% to 70% of their 1-RM, and they performed 3 to 4 sets of 10 to 15 repetitions of both exercises. During the third and fourth months, the participants performed 8 to 12 "explosive" repetitions and 3 to 5 sets of 5 to 6 repetitions with 60% to 80% of their 1-RM for the "controlled" repetitions. The frequency of training during this period was twice per week. During the last 2 months of training, the participants also performed 8 to 12 repetitions of "explosive" knee extensions with 50% to 60% of their 1-RM and then performed 4 to 6 sets of 3 to 6 repetitions with 70% to 80% of their 1-RM for the remaining exercise. The frequency was again twice per week. The participants' 1-RM was reassessed and adjusted every second month during this research. Testing performed at the end of the 6-month program demonstrated that the force production of the quadriceps femoris muscles in these participants increased by 30% to 60%, although their CSA increased to a lesser degree. (33)

[FIGURE 3 OMITTED]

Harridge et al (34) enrolled participants who were very old (age = 85-97 years) in a quadriceps femoris muscle training program in which participants performed progressive resistive training 3 times per week for 12 weeks. During the first week of training, the participants performed 3 sets of 8 knee extensions with a load of 50% of their 1-RM. During weeks 2 through 12, the participants performed 3 sets of knee extensions with a load of 80% of their 1-RM. The participants' 1-RM was reassessed and adjusted every 2 weeks. After 3 months of training, the participants' quadriceps femoris muscle force production had increased by an average of 134%, whereas their lean CSA (contractile tissue only) had increased by 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 researchers (33,34,36,38) 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 authors (48-53) believe that aerobic exercises that load the lower extremities substantially (eg, running) and strength training help to prevent or slow osteoporosis 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. Researchers (48,49,52) 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.

Table.

A Sample Progressive Resistance Training Program

Period of     No. of            Training
Training      Repetitions       Intensity

Weeks 1-3     3 sets of 8-15    50%-60% of 1-RM (a)
Weeks 4-8     3 sets of 8-10    60%-75% of 1-RM
Weeks 9-12    3 sets of 4-6     75%-90% of 1-RM

* 1-RM=one-repetition maximum.

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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) ([e-mail]). 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.