Age-related loss of skeletal muscle mass (ie, senile sarcopenia) leads to an increased risk of several diseases and mortality as well as reduced physical functioning and may eventually result in the loss of functional independence.1,2 The etiology of sarcopenia is multifactorial and complex. Several factors have been implicated and include declining anabolic hormone concentrations,3 nutritional deficiencies,4 chronic inflammation,5 and insulin resistance.6 Decreased physical activity levels that occur with aging also contribute to sarcopenia. It is well established that hormonal receptors for mRNA and transcriptional activity are increased7 and that there is reduced insulin resistance8 in exercising muscles following an acute bout of exercise for sedentary individuals. There are therefore many important interrelationships between physical activity levels and other etiologic factors associated with health and aging that may contribute in varying degrees to the age-related loss of skeletal muscle mass in older men and women.
Age-related loss of skeletal muscle mass has been studied extensively by evaluating muscle volume or muscle cross-sectional area (CSA).9 Janssen et al10 reported that skeletal muscle loss with increased age is greater in the lower limbs than in the upper extremities and is primarily associated with decreased use of the lower extremities in activities such as walking. We recently demonstrated that age is associated with site-specific loss of skeletal muscle mass in men and women aged 20 to 95 years.11 Interestingly, in the anterior and posterior regions of the thigh, age-related muscle loss was observed in the quadriceps but not in the posterior region. The cause of age-related, site-specific muscle loss is still unknown. However, it is possible that daily physical activities as well as sports are highly dependent on different muscle groups located both centrally in the trunk and peripherally in the limbs of the upper and lower body. According to previous studies,12 appendicular muscle mass and strength losses with increasing age can be attenuated by resistance exercise in healthy older adults. We hypothesized that the site-specific loss of skeletal muscle mass is probably associated with the decline in moderate- and/or high-intensity physical activities that occurs with increasing age. However, it is unknown whether habitual sports and exercise activity is associated with age-related, site-specific loss of muscle mass. The purpose of this study was to compare the size distribution of age-related loss of muscle size between habitually active and inactive young and old Japanese women.
A total of 309 women were recruited for this cross-sectional study. Of these, 152 were young (aged 20–34 years) and 157 were old (aged 60–85 years). Both young and old women were classified into 4 subgroups on the basis of their habitual (more than once a week) recreational exercise and sports activity: young active (n = 86), young inactive (n = 66), old active (n = 43), and old inactive (n = 114) groups. Before obtaining informed consent, a written description of the purpose of the study and its safety was distributed to potential participants, along with a lifestyle questionnaire. All participants were free of overt chronic disease (diabetes, angina, myocardial infarction, cancer, stroke, etc) as assessed by self-report. Candidates with clinically relevant cardiovascular or musculoskeletal disease, as well as those with cancer or previous stroke, were excluded from the study. The study was conducted according to the Declaration of Helsinki and was approved by the Ethics Committee for Human Experiments of the University of Tokyo, Tokyo, Japan.
Assessments of Body Mass Index and Body Composition
Body mass and standing height were measured to the nearest 0.1 kg and 0.1 cm, respectively, by using a height scale and an electronic weight scale. Body mass index was defined as body mass (kg)/height2 (m2). Selected anthropometric measures were obtained bilaterally from all participants: humerus, femur, and tibial lengths, and hip and waist circumferences, as described previously.13 Percent body fat was estimated from subcutaneous fat thickness by using an ultrasound-derived prediction equation,13 and fat-free mass (FFM) was calculated.
Measurements of Site-Specific Muscle Size
Muscle size was measured using B-mode ultrasound (Aloka SSD-500, Tokyo, Japan) at 8 anatomic sites on the anterior and posterior aspects of the body (biceps, triceps, abdomen, the area inferior to the scapula [hereinafter called “subscapula”], quadriceps, hamstrings, tibialis anterior, and triceps surae), as has been described previously.13 The measurements were taken while the individuals stood with their elbows and knees extended and relaxed. A 5-MHz scanning head was placed on a measurement site without depressing the dermal surface. The subcutaneous adipose tissue-muscle interface and the muscle-bone interface were identified from the ultrasonic image (Figure 1), and the distance between the 2 interfaces was recorded as muscle thickness (MTH). Previous studies have reported that MTH is strongly correlated with muscle CSA in limb and trunk muscles.14,15 The MTH was expressed in terms relative to limb length (MTH/L) or standing height (MTH/Ht).
Sociodemographic and lifestyle characteristics (age, gender, race, alcohol consumption, smoking status, and habitual physical activity) were considered potential confounders of the relationship between site-specific muscle loss and physical activity in both age groups.
The differences between the younger and older women and between the 4 physical activity subgroups (young active, young inactive, old active, and old inactive) were tested for significance by 1-way analysis of variance (ANOVA). Where the analysis revealed a significant difference, individual paired t tests were used with a Fisher least significant difference test to determine the origin of such effects. In the present study, we focused on comparing the young inactive subgroup with the old active subgroup to determine whether muscle size would be similar between the 2 subgroups when habitual sports and exercise activities were effective for old women. Results are expressed as means and standard deviation (mean ± SD) for all variables. P values < .05 were considered statistically significant.
Habitual Recreational Exercise and Sports
The rates of habitual recreational exercise and sports activities in the younger and older women were 56.6% and 27.4%, respectively. The main types of activities were aerobic dance, swimming, and weight training for the younger women, and walking, gateball, and gymnastic exercises and stretching for the older women. The frequency of exercise and sports was higher in the older women, but the duration was longer in the younger women (Table 1). The smoking rate was higher in the younger women (18%) than in the older women (2%), while the average number of cigarettes smoked per day was similar in both groups. The drinking rate (at least 1 drink per week) was higher in the younger women (39%) than in the older women (14%).
Age-Related, Site-Specific Muscle Loss
Body mass and FFM were similar between the younger and older women. The older women had lower quadriceps MTH/L, abdomen MTH/Ht, and triceps surae MTH/L than the younger women. On the contrary, the hamstrings MTH/L, subscapula MTH/Ht, and biceps MTH/L were higher in the older women, while the triceps MTH/L and tibialis anterior MTH/L were similar between the older and younger women. Similar results were found between the young inactive and old inactive subgroups and between the young active and old active subgroups. Body mass index and percent body fat were higher in the older women than in the younger women.
Effect of Habitual Recreational Activity
There were no significant differences in body mass and FFM between the young active (mean [SD] = 52.4 [5.9] kg and 39.7 [3.8] kg, respectively) and young inactive (mean [SD] = 51.8 [6.7] kg and 38.8 [4.0] kg, respectively) women and between the old active (mean [SD] = 52.2 [6.6] kg and 38.2 [3.6] kg, respectively) and old inactive (mean [SD] = 52.3 [6.4] kg and 38.8 [3.8] kg, respectively) women. In both the younger and older women, the quadriceps MTH/L and triceps MTH/L were higher in the active women than in the inactive women, while the biceps MTH/L, subscapula MTH/Ht, and triceps surae MTH/L were similar between those 2 groups. On the contrary, the abdomen MTH/Ht, hamstrings MTH/L, and tibialis anterior MTH/L were higher in the young active women than in the young inactive women but were similar between the old active women and the old inactive women. The quadriceps MTH/L and abdomen MTH/Ht were lower in the old active women than in the young inactive women, while hamstrings MTH/L, subscapula MTH/L, biceps MTH/L, and triceps MTH/L were higher (Figures 2 and 3).
The current cross-sectional study had a relatively small sample size composed only of women, but the results are consistent with those of our previous large sample size study,11 which found that the age-related loss of skeletal muscle mass is site-specific, especially for the quadriceps and abdominal muscles. Our results coincide with those of a longitudinal study16 that reported significant reductions in total and anterior thigh muscle CSA after an 8.9-year follow-up, while the posterior muscle group did not change. Considering the etiology of sarcopenia, age-related declines in androgen concentrations may be a strong influencing factor.3 The circulating androgens act to target tissue through specific hormone receptors that are upregulated in exercising muscle, but not in nonexercising muscle, following an acute bout of exercise. If one accepts the notion of a homogeneous loss of muscle tissue with increasing age owing to common etiologic factors, it is difficult to explain the site-specific muscle loss that we reported in the present study. Thus, age-related, site-specific muscle loss is probably the result of an interrelationship between physical activity levels and other etiologic factors.
In this study, greater muscle size was found in active young women in several muscle sites compared with inactive young women, suggesting that habitual (more than once a week) exercise and sports activities, mainly aerobic dance, swimming, and weight training, elicit muscle hypertrophy. On the contrary, quadriceps muscle size was greater in active old women, but the hamstrings muscle size did not differ between active and inactive women because there was no age-related muscle loss in the hamstrings. Although age-related, site-specific muscle loss is still observed, our results indicated that low- and moderate-intensity physical activity (our older participants performed mainly walking, gateball, and gymnastic exercises) may prevent age-related loss of quadriceps muscle but not abdominal muscle in older women.
In this study, we focused on comparing the younger inactive subgroup with the older active subgroup to determine whether muscle size would be similar between the 2 subgroups when habitual sports and exercise activities were effective for older women. Our results showed that the older active women had lower quadriceps or abdominal muscle size than the younger inactive women. Previous studies17,18 reported that the muscle activation patterns during daily physical activity are similar between the vastus lateralis and hamstrings muscles, although the activation levels are different. Compared with young adults, however, the exercise intensities associated with performing daily activities are increased in older populations owing in part to decreasing muscular strength that is associated with increasing age.19 Daily activities that are associated with high or relatively moderate loads, such as squatting and trunk curls, are usually not part of the normal daily pattern of activities for middle-aged and older adults; as a result, site-specific muscle loss, especially in the quadriceps and abdominal muscles, may occur with increased age. Since previous studies12,20 have reported that muscle mass and strength losses associated with increasing age can be attenuated by resistance training, at least in healthy older individuals, the exercise intensity and/or duration of daily physical activities may be an important influencing factor for sarcopenia-induced, site-specific muscle loss. Thus, to prevent or reverse quadriceps and abdominal muscle loss, which is most obvious as age-related, site-specific muscle loss, relatively higher-intensity exercise, such as squatting and trunk curls, is needed for healthy older Japanese women.
The results of this cross-sectional study showed that the muscle size of the biceps, subscapula, and hamstrings was greater in the older women than in the younger women, while the size of the quadriceps and abdominal muscles was low in the older women than in the younger women. As a result, there was no difference in FFM between the younger and older women. Previous studies21,22 have reported that an age-related decline in FFM in women usually occurs after the sixth decade of life, with the magnitude of the decline smaller in women than in men. Nassis and Geladas23 reported an age-related increase in body fat with no detectable change in FFM in women aged 18 to 69 years. From our results, it seems that age-related changes in muscle mass do occur, with several muscles losing mass and others gaining mass, while the total body muscle mass remains unchanged. The site-specific muscle loss may be associated with lifestyle factors, including changes in endocrine secretion, nutrition, and physical activity (eg, intensity and mode of exercise). Further study is needed to determine the etiologic factors associated with site-specific quadriceps and abdominal muscle loss in older women.
In this study, we used an ultrasound technique to determine limb and trunk muscle size. However, it is not possible to measure the potential contribution of nonmuscle tissue to total muscle size, using ultrasound. An increase in nonmuscle tissue in older muscle has been reported. A previous study24 reported a 59% increase in nonmuscle tissue for the quadriceps and a 127% increase in nonmuscle tissue for the hamstrings in older subjects compared with younger subjects. The absolute values of nonmuscle tissue in younger and older subjects were 3.2 and 5.1 cm2, respectively, for the quadriceps, and 2.2 and 5.0 cm2, respectively, for the hamstrings. Although older subjects in this study may have more nonmuscle tissue than younger subjects, we cannot explain the site-specific muscle loss in mass.
Our results indicate that age-related muscle loss remains site-specific in both active and inactive young and old women, even when habitual physical activity has an effect on muscle size.
The authors thank the individuals who participated in this study.
1. Rantanen T. Muscle strength, disability and mortality. Scand J Med Sci Sports. 2003;13:3–8.
2. Sowers MF, Crutchfield M, Richards K, et al. Sarcopenia is related to physical functioning and leg strength in middle-aged women. J Gerontol A Biol Sci Med Sci. 2005;60:486–490.
3. Morley JE. Hormones and the aging process. J Am Geriatr Soc. 2003;51:S333–S337.
4. Morley JE, Baumgartner RN, Roubenoff R, Mayer J, Nair KS. Sarcopenia. J Lab Clin Med. 2001;137:231–243.
5. Cesari M, Kritchevsky SB, Baumgartner RN, et al. Sarcopenia, obesity, and inflammation—results from the Trial of Angiotensin Converting Enzyme Inhibition and Novel Cardiovascular Risk Factors study. Am J Clin Nutr. 2005;82:428–434.
6. Guillet C, Boirie Y. Insulin resistance: a contributing factor to age-related muscle mass loss? Diabetes Metab. 2005;31:5S20–5S26.
7. Willoughby DS, Taylor L. Effects of sequential bouts of resistance exercise on androgen receptor expression. Med Sci Sports Exerc. 2004;36:1499–1506.
8. Black LE, Swan PD, Alvar BA. Effects of intensity and volume on insulin sensitivity during acute bouts of resistance training. J Strength Cond Res. 2010;24:1109–1116.
9. Doherty TJ. Invited review: aging and sarcopenia. J Appl Physiol. 2003;95:1717–1727.
10. Janssen I, Heymsfield SB, Wang Z, Ross R. Skeletal muscle mass and distribution in 468 men and women aged 18–88 yr. J Appl Physiol. 2000;89:81–88.
11. Abe T, Sakamaki M, Yasuda T, et al. Age-related, site-specific muscle loss in 1507 Japanese men and women aged 20 to 95 years. J Sports Sci Med. 2011;10:145–150.
12. Frontera WR, Meredith CN, O'Reilly KP, Knuttgen HG, Evans WJ. Strength conditioning in older men: skeletal muscle hypertrophy and improved function. J Appl Physiol. 1988;64:1038–1044.
13. Abe T, Kondo M, Kawakami Y, Fukunaga T. Prediction equations for body composition of Japanese adults by B-mode ultrasound. Am J Hum Biol. 1994:6:161–170.
14. Abe T, Kawakami Y, Suzuki Y, Fukunaga T, Gunji A. Effects of 20 days of bed rest on muscle morphology. J Gravit Physiol. 1997;4:S10–S14.
15. Sanada K, Kearns CF, Midorikawa T, Abe T. Prediction and validation of total and regional skeletal muscle mass by ultrasound in Japanese adults. Eur J Appl Physiol. 2006;96:24–31.
16. Frontera WR, Reid KF, Phillips EM, et al. Muscle fiber size and function in elderly humans: a longitudinal study. J Appl Physiol. 2008;105:637–642.
17. Sawai S, Sanematsu H, Kanehisa H, Tsunoda N, Fukunaga T. Sexual-related difference in the level of muscular activity of trunk and lower limb during basic daily life actions. Jpn J Phys Fitness Sports Med. 2006;55:247–257.
18. Shirasawa H, Kanehisa H, Kouzaki M, Masani K, Fukunaga T. Differences among lower leg muscles in long-term activity during ambulatory condition without any moderate to high intensity exercise. J Electromyogr Kinesiol. 2009;19:e50–e56.
19. Takai Y, Sawai S, Kanehisa H, Kawakami Y, Fukunaga T. Age and sex differences in the levels of muscular activities during daily physical actions. Int J Sport Health Sci. 2008;6:169–181.
20. Ferri A, Scaglioni G, Pousson M, Capodaglio P, Van Hoecke J, Narici MV. Strength and power changes of the human plantar flexors and knee extensors in response to resistance training in old age. Acta Physiol Scand. 2003;177:69–78.
21. Guo SS, Zeller C, Chumlea WC, Siervogel RM. Aging, body composition, and lifestyle: the Fels Longitudinal Study. Am J Clin Nutr. 1999;70:405–411.
22. Kyle UG, Genton L, Hans D, Karsegard L, Slosman DO, Pichard C. Age-related differences in fat-free mass, skeletal muscle, body cell mass and fat mass between 18 and 94 years. Eur J Clin Nutr. 2001;55:663–672.
23. Nassis GP, Geladas ND. Age-related pattern in body composition changes for 18–69 year old women. J Sports Med Phys Fitness. 2003;43:327–333.
24. Overend TJ, Cunningham DA, Paterson DH, Lefcoe MS. Thigh composition in young and elderly men determined by computed tomography. Clin Physiol. 1992;12:629–640.
body composition; muscle thickness; sarcopenia; ultrasound© 2011 Academy of Geriatric Physical Therapy, APTA