Objectively Measured Physical Activity and Progressive Loss of Lean Tissue in Older Japanese Adults: Longitudinal Data from the Nakanojo Study Roy J. Shephard, MD, PhD, DPE, LLD,* Hyuntae Park, PhD,† Sungjin Park, MSc,† and Yukitoshi Aoyagi, PhD†
OBJECTIVES: To relate 5-year lean tissue loss to habitual physical activity of elderly adults. DESIGN: Longitudinal. SETTING: Community of Nakanojo. PARTICIPANTS: Community-living Japanese aged 65 to 84 (200 men, 268 women). MEASUREMENTS: Daily 24-hour pedometer/accelerometer data, collected continuously for 5 years, were categorized into activity quartiles. Bioelectrical impedance measurements of lean body mass were taken annually. A sarcopenia threshold was defined arbitrarily as an appendicular lean mass/height2 of more than 1 standard deviation below the mean for healthy young Japanese. RESULTS: Subjects with greater habitual physical activity retained a greater lean mass over the 5 years of observation. Controlling for baseline lean mass and age, final lean mass was greater for the third activity quartile (men and women with respective mean counts of 7,800 and 7,700 steps per day or mean duration of exercise at >3 metabolic equivalents (METs) of 20 and 17 minutes per day) than for the first and second quartiles. A multivariate-adjusted proportional hazards model predicted that, over the 5 years, men and women in the two lowest activity quartiles (8,400 steps per day). Likewise, men and women with less than 16 and less than 14 minutes per day, respectively, of activity of more than 3 METs were 3.0 (95% CI = 2.0– 6.0) and 3.5 (95% CI = 2.1–6.3) times as likely to develop sarcopenia as those with more than 28 and more than 22 minutes per day. From the *Faculty of Kinesiology and Physical Education, University of Toronto, Ontario, Canada; and †Exercise Sciences Research Group, Tokyo Metropolitan Institute of Gerontology, Tokyo, Japan. Address correspondence to Yukitoshi Aoyagi, Exercise Sciences Research Group, Tokyo Metropolitan Institute of Gerontology, 35–2 Sakaecho, Itabashi-ku, Tokyo 173–0015, Japan. E-mail: [email protected] DOI: 10.1111/jgs.12505
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CONCLUSION: After adjustment for potential confounders, the risk of developing sarcopenia was substantially lower in elderly people taking at least 7,000 to 8,000 steps per day or exercising for at least 15 to 20 minutes per day at an intensity greater than 3 METs. Clinicians should encourage seniors to get at least this volume of regular daily exercise. J Am Geriatr Soc 61:1887–1893, 2013.
Key words: accelerometer; aging; moderate-exercise duration; sarcopenia; step count
S
arcopenia is an age-related condition characterized by loss of muscle mass, with a concomitant decline in maximal voluntary force, loss of muscle power, tendency to tire, vulnerability to falls, and onset of dependency.1–5 Many epidemiological studies6–8 have shown negative relationships between habitual physical activity and sarcopenia, and there is also evidence of a potential to reverse at least some of this muscle loss, even in institutionalized elderly adults, through an appropriate resistance exercise regimen,9 but the optimal intensity and total amount of activity for the preservation of muscle function in community-living seniors remain unclear. One major problem hampering the development of effective public health policy recommendations is that most investigators have examined physical activity patterns using subjective questionnaires or accelerometer or pedometer measurements limited to a period of 1 week or less, despite recognition of the fallibility of questionnaires, problems arising from changes in physical activity patterns with season and weather conditions, and the short-term stimulation of activity patterns associated with the wearing of monitoring devices or the reporting of activity patterns.10–12 In this context, a previous study with yearlong pedometer/accelerometer measurements of habitual physical activity8 demonstrated that elderly individuals who
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took an average of at least 7,000 steps per day and spent an average of 19 minutes per day in activity at an intensity of more than 3 metabolic equivalents (METs) did not demonstrate a dual-energy X-ray absorptiometry (DXA)-based index typical of sarcopenia, whereas the average daily activity of those whose DXA values fell below the sarcopenia threshold was much lower (5,100 steps per day and 12 minutes per day at >3 METs). Nevertheless, the fitting of exponential curves to the data suggested that benefit plateaued at counts of approximately 8,000 steps per day or approximately 22 minutes per day of moderate exercise in men and 6,900 steps per day or 19 minutes per day of moderate exercise in women. A cross-sectional study of this type cannot prove a causal relationship between regular physical activity and the prevention of sarcopenia. Accordingly, a 5-year prospective study of elderly Japanese men and women who initially had an acceptable lean tissue mass, above the sarcopenia threshold, was initiated. The objectives were to examine relationships between objective pedometer/ accelerometer assessments of the amount and intensity of habitual physical activity undertaken and the overall loss of lean tissue mass as assessed according to repeated bioimpedance measurements and to compare the risk of lean tissue mass dropping below the sarcopenia threshold in subjects with differing levels of habitual physical activity.
METHODS Subjects Subjects were 468 community-living Japanese volunteers aged 65 to 84 (200 men, 268 women), all residents of Nakanojo (population ~18,000). Participants provided written informed consent to participate in this institutionally approved investigation after the protocol and possible risks had been fully explained to them. All had completed a detailed medical examination as a part of the overall Nakanojo Study. They were ambulatory, with initial bioimpedance scores above the sarcopenia threshold, and without evidence of orthopedic problems, cognitive impairment, specific myopathies, or chronic or terminal illness that could have affected the variables under investigation. All of the subjects who were initially selected completed the 5-year study.
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After inspection of printouts for periods of inappropriate data recording, step counts and intensity categories were totaled over each 24-hour period from midnight to the following midnight. Procedures for addressing missing data have been discussed previously.12 A high degree of cooperation was obtained from the subjects; all of the 468 participants provided records with less than 5% of data missing for each of the five Julys studied. Summary parameters calculated for the present study were the number of steps taken per day and the daily duration of exercise of more than 3 METs. For the purpose of the present study, both indices were averaged throughout each of five Julys. The month of July was selected for the analysis because, in Nakanojo, pedometer/accelerometer counts for this month are representative of data for elderly subjects throughout the entire year,14 and 1 month of observations provides sufficient data to predict yearlong physical activity with greater than 80% reliability.19
Lean Body Mass Measurements Bioelectrical impedance measurements of appendicular lean body mass (bioimpedance analyzer MC-190, Tanita Corp., Itabashi, Tokyo, Japan) were made at baseline and at the end of each succeeding year. Subjects stood barefoot on the analyzer platform grasping the two hand grips. The instrument uses multiple-frequency (5, 50, 250, and 500 kHz) bioimpedance technology. Eight tactile electrodes make contact with the palm and thumb of each hand and with the anterior and posterior aspects of the sole of each foot. Surface electrodes are placed on the right side of the body, on the dorsal surface of the hands and feet proximal to the metacarpal- and metatarsal-phalangeal joints, respectively, and medially between the distal prominences of the radius and ulna and between the medial and lateral malleoli at the ankle. The scores obtained correspond to some 40% of total lean mass, which was termed appendicular lean mass. Sarcopenia (classes I and II) was declared if the estimate of appendicular lean mass/height2 fell more than 1 standard deviation (SD) below the corresponding mean value for a young, healthy reference population.5 Specific cutoff values were thus 9.37 kg/m2 in men and 7.01 kg/m2 in women, substantially higher than the limits adopted in a previous study.20
Statistical Analyses Physical Activity Measurements Details of the procedures for measuring physical activity have been described previously.13,14 In brief, an electronic pedometer/accelerometer with a storage capacity of 36 days (modified Kenz Lifecorder, Suzuken Co., Ltd., Nagoya, Aichi, Japan) was attached to a waist belt on the side of the body. Under laboratory conditions, this instrument can determine step counts with an intramode reliability of 0.998 and an accuracy of less than 3% of the actual number of steps taken.15–18 Subjects wore the device 24 hours per day for 5 years, providing a record of the number of steps taken and the intensity of physical activity every 4 seconds throughout each day. Monthly visits to the Nakanojo Public Health Center allowed data retrieval and battery replacement in the space of a few minutes.
All data were analyzed using SPSS 19.0 (SPSS Inc., Chicago, IL) or SAS 9.1 (SAS Institute, Inc., Cary, NC). Data are presented as means SDs. Nonpaired t-tests were used to compare the baseline physical characteristics, muscle mass, and habitual physical activity of men and women. Repeated-measure analyses of variance were used to test for possible changes in month-averaged physical activity scores between years. Subjects were divided arbitrarily into increasing quartiles (Q1–Q4) of average physical activity to test for possible statistical associations between levels of habitual physical activity and muscle mass. Analyses of covariance (ANCOVAs) were used to assess independent associations between the four categories of physical activity thus defined and the appendicular muscle mass at Years 1 to 5 after controlling for baseline lean
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step counts, there was a 2.3 (95% confidence interval (CI) = 1.4–4.5) times difference in risk in men and a 3.0 (95% CI = 1.9–3.4) times difference in women, and in terms of time spent at an intensity of greater than 3 METs, a 3.0 (95% CI = 2.0–6.0) times difference in risk in men and a 3.5 (95% CI = 2.1–6.3) times difference in women, but there was no significant difference in the 5-year risk of sarcopenia between the two highest quartiles (Q3 and Q4). Log-rank testing of Kaplan–Meier plots based upon physical activity quartiles showed significant interquartile differences with respect to the proportion of subjects remaining above the sarcopenia threshold over the 5 years of observation (Figure 1).
tissue mass and age. The Cochran-Armitage test was used to assess trends in loss of lean mass over time for subjects in each physical activity quartile; if trends were significant, the Williams correction was applied when comparing baseline scores with values for Years 1 to 5. Cox proportional hazards regression analysis was used to assess independent relationships between habitual physical activity values and the 5-year risk that lean mass would drop below the sarcopenia threshold, after controlling for baseline lean tissue mass, age, smoking status and alcohol consumption. A Kaplan–Meier plot was used to determine the proportion of subjects in each activity quartile who remained above the sarcopenia threshold in each year of the 5-year follow-up, and log-rank tests were used to analyze the statistical significance of differences in curves between physical activity quartiles. All statistical contrasts were made at the .05 level of significance.
DISCUSSION The present longitudinal study confirms the findings of previous cross-sectional observations:8 older adults with high pedometer/accelerometer scores have greater conservation of lean tissue than individuals who are more sedentary. It further demonstrates that the more-active subjects gain substantial protection against the risk of dropping below a specified sarcopenia threshold over 5 years of follow-up. Nevertheless, a few subjects even in the highest initial quartile of pedometer/accelerometer readings had a lean tissue mass indicative of appendicular sarcopenia at the end of the 5-year study. It remains to be clarified why these individuals were particularly vulnerable to the normal age-related loss of lean tissue, despite having apparently adequate amounts of regular physical activity. Possible explanations include differences of constitution and nutrition, side-effects of medication, and the onset of chronic disease. The body composition data for the longitudinal study were obtained by measuring electrical impedance; with the electrode placement used, the resulting index reflected some 40% of the individual’s total lean tissue mass. In a previous cross-sectional analysis,8 whole-body DXA measurements allowed loss of lean tissue from specific body regions (arm, leg, and combined appendicular sarcopenia) to be distinguished. Some limitations of bioimpedance data have been discussed in an earlier monograph.21 Bioimpedance has less absolute accuracy than DXA, but recent research22,23 shows satisfactory concordance in mean estimates of appendicular mass between the two methods when using the latest types of equipment. Although the prevalence of sarcopenia in the study population was
RESULTS Baseline characteristics showed the anticipated differences in height and body mass between men and women (P < .05); the two groups did not differ significantly with respect to age or body mass index (BMI), but both were substantially shorter than the current generation of North American older adults (Table 1). Moreover, no statistically significant sex differences were observed in the two chosen indices of habitual physical activity: 5-year average daily step count and 5-year average daily duration of exercise at more than 3 METs. As expected, initial lean tissue mass was substantially greater in men than in women. Subjects maintained a surprisingly constant level of physical activity over the 5 years of observation (Table 2). Lean tissue indices were greater for those with higher physical activity scores, more markedly for exercise duration at more than 3 METs than for step count (Table 3), although ANCOVA adjusted for baseline lean tissue mass and age showed no significant difference between the third and fourth activity quartiles. The Cochran-Armitage test showed no significant 5-year loss of lean tissue in either of the two highest activity quartiles (Q3 and Q4). A multivariate-adjusted Cox proportional hazards model predicted that, over the 5-year period of observation, the risk that an individual’s appendicular lean tissue mass would drop below the sarcopenia threshold was much greater for those in the two lowest activity quartiles than for those in the highest quartile (Table 4). In terms of
Table 1. Anthropometric Characteristics, Habitual Physical Activity Patterns, and Appendicular Lean Tissue Mass Indices of Subjects at Entry to Study Characteristic
Age Body mass, kg Height, m Body mass index, kg/m2 Appendicular lean tissue mass, kg/m2 Five-year average step count, steps/d Five-year average duration of physical activity >3 metabolic equivalents, min/d
Men, n = 200
73.5 54.9 1.55 22.8 11.5 6,937 16.8
4.3 10.3 0.21 3.2 2.3 2,312 6.4
Women, n = 268
P-Value for Difference
.43 .004 3 METs Q1 3.8 1.6 Q2 11.3 2.5 Q3 20.2 3.2 Q4 32.0 7.1 Women (n = 67/quartile) Steps per day Q1 3,481 937 Q2 5,703 781 Q3 7,513 713 Q4 10,361 1,621 Min/d of physical activity at >3 METs Q1 3.9 2.0 Q2 10.2 1.9 Q3 16.3 2.2 Q4 30.8 6.9
3
3,719 6,222 7,901 10,931
1,016 883 938 1,610
3.9 11.8 21.2 31.1
1.9 2.1 2.9 6.9
3,791 5,343 7,751 10,251
899 961 691 1,355
3.9 9.9 17.4 32.1
1.8 2.5 2.3 7.8
3,970 6,187 7,689 11,351
1,176 919 903 1,228
4.1 10.8 19.6 33.3
2.0 2.5 2.8 9.8
3,893 5,788 7,726 11,031
991 953 673 1,613
4.0 10.5 17.8 32.9
1.9 2.2 2.1 7.0
4,081 6,128 7,898 10,971
1,131 1,421 927 1,287
4.0 10.0 20.5 32.4
1.9 2.7 3.1 8.8
4,037 5,981 7,931 10,251
1,015 993 851 1,531
4.0 10.9 17.7 32.8
1.5 2.5 2.3 8.4
4,002 6,002 7,923 10,186
1,021 961 794 1,263
4.0 10.5 21.0 31.0
1.9 2.4 3.9 7.7
4,024 5,716 7,556 10,098
1,103 875 788 1,781
4.2 10.9 16.9 30.3
1.9 2.6 2.4 8.1
4,107 5,649 7,600 10,001
1,017 973 924 1,519
.27 .58 .63 .72
3.9 10.4 19.9 30.6
2.0 2.8 4.0 8.2
.21 .57 .77 .64
4,103 5,864 7,683 9,997
1,102 1,021 819 1,462
.19 .53 .66 .71
3.8 11.4 18.0 29.9
1.9 3.6 2.5 7.9
.43 .59 .78 .71
In men, average steps per day: Q1, range 1,294–5,517, 3,899 1,026; Q2, range 5,519–6,731, 6,019 782; Q3, range 6,741–8,978, 7,801 1,052; Q4, range 8,983–16,513, 10,660 1,584 and average min/d of moderate-intensity activity: Q1, range 0.7–7.8, 4.0 1.9; Q2, range 7.9–15.6, 10.9 2.5; Q3, range 15.7–27.9, 20.4 4.1; Q4, range 27.9–70.3, 31.7 11.3. In women, average steps per day: Q1, range 1,360–4,961, 3,887 1,321; Q2, range 4,981–6,841, 5,733 868; Q3, range 6,849–8,331, 7,693 831; Q4, range 8,387–16,918, 10,331 1,671 and average min/d of moderate-intensity activity: Q1, range 0.2–7.9, 4.0 2.3; Q2, range 8.0–14.0, 10.7 2.1; Q3, range 14.1–21.9, 17.4 3.3; Q4, range 22.0–55.8, 31.5 12.9.
similar when based on each of these three statistics, the correlation with pedometer/accelerometer measurements of physical activity was closer for appendicular and leg lean tissue mass than for the arms. Alternatively, a comparison of sarcopenic and nonsarcopenic individuals showed a greater deficiency of lean tissue in the arms (34%) than in the legs (17%). The total volume of lean tissue measured using the DXA method was smaller than that examined using the impedance technique, but the overall conclusions with respect to the benefits of habitual physical activity were similar. The definition of dose-response relationships linking habitual physical activity and some aspect of health such as lower risk of sarcopenia remains challenging. Some authors have postulated that a minimum threshold intensity of activity is needed to obtain any benefit, but others have suggested that the greatest benefit is seen in those who move from a totally sedentary lifestyle to a minimal amount of regular physical activity.24 Much presumably depends upon the population tested; their initial health, fitness, and state of nutrition; and the type of exercise undertaken. Strengths of the present investigation include its longitudinal design, its long duration, and the objective measurement of physical activity, although the study was restricted to one specific community, differing from North America in respect to the sociocultural environment and patterns of medical care. The Japanese subjects were also much shorter and less obese than would be
anticipated in North American seniors, possibly implying lower protein and energy intake over part or all of their lifespan; in such a population, part of the apparent advantage of lean tissue mass seen in an individual with a high level of physical activity could reflect greater food intake than that of his or her peers, with a corresponding greater availability of essential amino acids for synthesis of muscle tissue.25 The pedometer/accelerometer used provides a good objective index of endurance activities such as walking, which was the main source of exercise for most subjects, although the device may be less responsive to resistance exercise, and it is possible that the observed correlations do not reflect the volume of exercise required to protect against sarcopenia. Rather, the study may have identified the more-active members of the community who engage in endurance activity (which as measured) and resistance activity (which the measuring device did not assess). The method used to determine lean body mass and thus sarcopenia (bioimpedance) was appropriate for the number of field assessments required, but it is less precise than some laboratory techniques, does not assess regional lean tissue mass, and reflects only a part of total lean tissue. Moreover, age-related changes in tissue hydration could have influenced the bioimpedance data. A consensus panel meeting in Rome in November 200920 proposed functional criteria of sarcopenia (e.g., being bedridden, being unable to rise independently from a chair, or having
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Table 3. Appendicular Lean Tissue Mass Indices for Initial Visit (Baseline) and for Each of 5 Succeeding Years, Classified According to Quartile (Q1–Q4) of Habitual Physical Activity Baseline
1
2
3
4
5 P-Value for Trend
Mean Standard Deviation
Subject Category
Men (n = 50/quartile) Step count Q1 10.5 2.0 Q2 11.5 1.9 Q3 11.4 2.0 Q4 12.5 1.9 Duration of physical activity at >3 METs Q1 10.3 1.6 Q2 11.1 2.3 Q3 11.8 1.8 Q4 12.7 2.1 Women (n = 67/quartile) Step count Q1 8.0 2.1 Q2 8.8 1.6 Q3 8.9 2.3 Q4 9.5 2.1 Duration of physical activity at >3 METs Q1 7.9 1.8 Q2 8.3 2.1 Q3 9.2 1.8 Q4 9.8 1.7
10.2 11.4 11.3 12.7
2.6 1.3 1.2 1.9
9.9 11.2 11.2 12.4
1.9 1.9 1.8 1.7
9.8 10.9 11.5 12.3
2.8a 1.5a 2.0 2.2
9.7 10.9 10.9 12.3
2.6a 1.4a 1.4 1.7
9.6 10.9 11.0 12.2
2.1a 2.0a 1.9 2.1
.01 .03 .18 .38
10.0 11.0 11.8 12.8
2.6 2.5 2.4 2.4
9.8 10.7 11.7 12.5
2.8 2.1 1.7 1.6
9.6 10.4 11.8 12.7
2.1a 1.8a 1.8 2.4
9.4 10.5 11.5 12.5
2.2a 2.1a 2.1 2.5
9.4 10.3 11.5 12.5
2.4a 2.5a 2.0 1.8
.02 .02 .28 .36
7.8 8.5 8.9 9.5
1.9 2.1 2.6 2.7
7.5 8.4 8.9 9.4
2.0a 2.5 2.6 2.1
7.6 8.3 8.6 9.4
1.9a 2.8 2.9 2.5
7.5 8.2 8.5 9.3
2.0a 2.1a 2.8 2.4
7.4 8.1 8.3 9.3
2.0a 1.9a 2.1 2.7
.03 .02 .17 .13
7.7 8.0 9.1 9.8
2.0 2.1 2.8 2.9
7.4 7.9 9.1 9.7
1.9a 2.1 2.7 3.0
7.3 7.8 9.0 9.7
1.7a 2.1a 2.6 2.7
7.2 7.6 9.0 9.6
1.9a 2.0a 2.3 2.6
7.0 7.6 8.8 9.6
2.1a 1.9a 2.4 2.6
.01 .03 .13 .27
For details of average step counts and average duration of moderate activity in the quartiles, see footnote to Table 2. a Difference from baseline (P < .05). MET = metabolic equivalent.
Table 4. Risk of Appendicular Lean Tissue Mass Index Falling Below the Arbitrary Sarcopenia Threshold over the 5-Year Study, Classified According to Quartile (Q1–Q4) of Habitual Physical Activity (Reference Q4) Men (n = 50/Quartile) Subject Category
Women (n = 67/Quartile)
Relative Risk (95% Confidence Interval)
Step count Q1 2.33 (1.43–4.51) 2.99 Q2 1.97 (1.00–2.86) 2.01 Q3 0.95 (0.43–2.01) 1.03 P-value for trend .04 .03 Duration of physical activity at >3 metabolic equivalents Q1 3.01 (2.02–5.99) 3.49 Q2 1.78 (1.32–4.17) 2.21 Q3 1.13 (0.57–2.15) 0.91 P-value for trend .01 .02
(1.91–3.42) (1.01–3.03) (0.58–2.25)
(2.11–6.32) (1.03–3.61) (0.37–2.51)
Values adjusted for baseline lean tissue mass, age, smoking status, and alcohol intake. For details of average step counts and average duration of moderate activity in the quartiles, see footnote to Table 2.
a measured gait speed of 3 METs) than with volume (daily step count). In this study, individuals in the two most active quartiles of physical activity (≥7,000–8,000 steps/d or ≥15–20 min/d of exercise at an intensity of >3 METs) had a lower probability of losing muscle mass over 5 years than those who were less active. Clinicians should encourage seniors to reach such levels of daily physical activity.
ACKNOWLEDGMENTS This article focuses particularly on data from an interdisciplinary study of the habitual physical activity and health of elderly people living in Nakanojo, Gunma, Japan (the Nakanojo Study). The authors gratefully acknowledge the expert technical assistance of the research and nursing staffs of the Tokyo Metropolitan
Institute of Gerontology, the University of Tokyo, and the Nakanojo Public Health Center. We also thank the subjects whose conscientious participation made the Nakanojo Study possible. Conflict of Interest: This study was supported in part by grants (Grant-in-Aid for Encouragement of Young Scientists 12770037 and Grant-in-Aid for Scientific Research [C]: 15500503, [C]: 17500493, [B]: 19300235, and [B]: 23300259) from the Japan Society for the Promotion of Science. Author Contributions: Roy J. Shephard: interpretation of data, preparation of manuscript. Hyuntae Park: acquisition of subjects and data, analysis of data, preparation of manuscript. Sungjin Park: acquisition of subjects and data. Yukitoshi Aoyagi: study concept and design, acquisition of subjects and data, analysis and interpretation of data, preparation of manuscript. Sponsor’s Role: None.
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OBJECTIVES: To relate 5-year lean tissue loss to habitual physical activity of elderly adults. DESIGN: Longitudinal. SETTING: Community of Nakanojo. PARTICIPANTS: Community-living Japanese aged 65 to 84 (200 men, 268 women). MEASUREMENTS: Daily 24-hour pedometer/accelerometer data, collected continuously for 5 years, were categorized into activity quartiles. Bioelectrical impedance measurements of lean body mass were taken annually. A sarcopenia threshold was defined arbitrarily as an appendicular lean mass/height2 of more than 1 standard deviation below the mean for healthy young Japanese. RESULTS: Subjects with greater habitual physical activity retained a greater lean mass over the 5 years of observation. Controlling for baseline lean mass and age, final lean mass was greater for the third activity quartile (men and women with respective mean counts of 7,800 and 7,700 steps per day or mean duration of exercise at >3 metabolic equivalents (METs) of 20 and 17 minutes per day) than for the first and second quartiles. A multivariate-adjusted proportional hazards model predicted that, over the 5 years, men and women in the two lowest activity quartiles (8,400 steps per day). Likewise, men and women with less than 16 and less than 14 minutes per day, respectively, of activity of more than 3 METs were 3.0 (95% CI = 2.0– 6.0) and 3.5 (95% CI = 2.1–6.3) times as likely to develop sarcopenia as those with more than 28 and more than 22 minutes per day. From the *Faculty of Kinesiology and Physical Education, University of Toronto, Ontario, Canada; and †Exercise Sciences Research Group, Tokyo Metropolitan Institute of Gerontology, Tokyo, Japan. Address correspondence to Yukitoshi Aoyagi, Exercise Sciences Research Group, Tokyo Metropolitan Institute of Gerontology, 35–2 Sakaecho, Itabashi-ku, Tokyo 173–0015, Japan. E-mail: [email protected] DOI: 10.1111/jgs.12505
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CONCLUSION: After adjustment for potential confounders, the risk of developing sarcopenia was substantially lower in elderly people taking at least 7,000 to 8,000 steps per day or exercising for at least 15 to 20 minutes per day at an intensity greater than 3 METs. Clinicians should encourage seniors to get at least this volume of regular daily exercise. J Am Geriatr Soc 61:1887–1893, 2013.
Key words: accelerometer; aging; moderate-exercise duration; sarcopenia; step count
S
arcopenia is an age-related condition characterized by loss of muscle mass, with a concomitant decline in maximal voluntary force, loss of muscle power, tendency to tire, vulnerability to falls, and onset of dependency.1–5 Many epidemiological studies6–8 have shown negative relationships between habitual physical activity and sarcopenia, and there is also evidence of a potential to reverse at least some of this muscle loss, even in institutionalized elderly adults, through an appropriate resistance exercise regimen,9 but the optimal intensity and total amount of activity for the preservation of muscle function in community-living seniors remain unclear. One major problem hampering the development of effective public health policy recommendations is that most investigators have examined physical activity patterns using subjective questionnaires or accelerometer or pedometer measurements limited to a period of 1 week or less, despite recognition of the fallibility of questionnaires, problems arising from changes in physical activity patterns with season and weather conditions, and the short-term stimulation of activity patterns associated with the wearing of monitoring devices or the reporting of activity patterns.10–12 In this context, a previous study with yearlong pedometer/accelerometer measurements of habitual physical activity8 demonstrated that elderly individuals who
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took an average of at least 7,000 steps per day and spent an average of 19 minutes per day in activity at an intensity of more than 3 metabolic equivalents (METs) did not demonstrate a dual-energy X-ray absorptiometry (DXA)-based index typical of sarcopenia, whereas the average daily activity of those whose DXA values fell below the sarcopenia threshold was much lower (5,100 steps per day and 12 minutes per day at >3 METs). Nevertheless, the fitting of exponential curves to the data suggested that benefit plateaued at counts of approximately 8,000 steps per day or approximately 22 minutes per day of moderate exercise in men and 6,900 steps per day or 19 minutes per day of moderate exercise in women. A cross-sectional study of this type cannot prove a causal relationship between regular physical activity and the prevention of sarcopenia. Accordingly, a 5-year prospective study of elderly Japanese men and women who initially had an acceptable lean tissue mass, above the sarcopenia threshold, was initiated. The objectives were to examine relationships between objective pedometer/ accelerometer assessments of the amount and intensity of habitual physical activity undertaken and the overall loss of lean tissue mass as assessed according to repeated bioimpedance measurements and to compare the risk of lean tissue mass dropping below the sarcopenia threshold in subjects with differing levels of habitual physical activity.
METHODS Subjects Subjects were 468 community-living Japanese volunteers aged 65 to 84 (200 men, 268 women), all residents of Nakanojo (population ~18,000). Participants provided written informed consent to participate in this institutionally approved investigation after the protocol and possible risks had been fully explained to them. All had completed a detailed medical examination as a part of the overall Nakanojo Study. They were ambulatory, with initial bioimpedance scores above the sarcopenia threshold, and without evidence of orthopedic problems, cognitive impairment, specific myopathies, or chronic or terminal illness that could have affected the variables under investigation. All of the subjects who were initially selected completed the 5-year study.
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After inspection of printouts for periods of inappropriate data recording, step counts and intensity categories were totaled over each 24-hour period from midnight to the following midnight. Procedures for addressing missing data have been discussed previously.12 A high degree of cooperation was obtained from the subjects; all of the 468 participants provided records with less than 5% of data missing for each of the five Julys studied. Summary parameters calculated for the present study were the number of steps taken per day and the daily duration of exercise of more than 3 METs. For the purpose of the present study, both indices were averaged throughout each of five Julys. The month of July was selected for the analysis because, in Nakanojo, pedometer/accelerometer counts for this month are representative of data for elderly subjects throughout the entire year,14 and 1 month of observations provides sufficient data to predict yearlong physical activity with greater than 80% reliability.19
Lean Body Mass Measurements Bioelectrical impedance measurements of appendicular lean body mass (bioimpedance analyzer MC-190, Tanita Corp., Itabashi, Tokyo, Japan) were made at baseline and at the end of each succeeding year. Subjects stood barefoot on the analyzer platform grasping the two hand grips. The instrument uses multiple-frequency (5, 50, 250, and 500 kHz) bioimpedance technology. Eight tactile electrodes make contact with the palm and thumb of each hand and with the anterior and posterior aspects of the sole of each foot. Surface electrodes are placed on the right side of the body, on the dorsal surface of the hands and feet proximal to the metacarpal- and metatarsal-phalangeal joints, respectively, and medially between the distal prominences of the radius and ulna and between the medial and lateral malleoli at the ankle. The scores obtained correspond to some 40% of total lean mass, which was termed appendicular lean mass. Sarcopenia (classes I and II) was declared if the estimate of appendicular lean mass/height2 fell more than 1 standard deviation (SD) below the corresponding mean value for a young, healthy reference population.5 Specific cutoff values were thus 9.37 kg/m2 in men and 7.01 kg/m2 in women, substantially higher than the limits adopted in a previous study.20
Statistical Analyses Physical Activity Measurements Details of the procedures for measuring physical activity have been described previously.13,14 In brief, an electronic pedometer/accelerometer with a storage capacity of 36 days (modified Kenz Lifecorder, Suzuken Co., Ltd., Nagoya, Aichi, Japan) was attached to a waist belt on the side of the body. Under laboratory conditions, this instrument can determine step counts with an intramode reliability of 0.998 and an accuracy of less than 3% of the actual number of steps taken.15–18 Subjects wore the device 24 hours per day for 5 years, providing a record of the number of steps taken and the intensity of physical activity every 4 seconds throughout each day. Monthly visits to the Nakanojo Public Health Center allowed data retrieval and battery replacement in the space of a few minutes.
All data were analyzed using SPSS 19.0 (SPSS Inc., Chicago, IL) or SAS 9.1 (SAS Institute, Inc., Cary, NC). Data are presented as means SDs. Nonpaired t-tests were used to compare the baseline physical characteristics, muscle mass, and habitual physical activity of men and women. Repeated-measure analyses of variance were used to test for possible changes in month-averaged physical activity scores between years. Subjects were divided arbitrarily into increasing quartiles (Q1–Q4) of average physical activity to test for possible statistical associations between levels of habitual physical activity and muscle mass. Analyses of covariance (ANCOVAs) were used to assess independent associations between the four categories of physical activity thus defined and the appendicular muscle mass at Years 1 to 5 after controlling for baseline lean
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step counts, there was a 2.3 (95% confidence interval (CI) = 1.4–4.5) times difference in risk in men and a 3.0 (95% CI = 1.9–3.4) times difference in women, and in terms of time spent at an intensity of greater than 3 METs, a 3.0 (95% CI = 2.0–6.0) times difference in risk in men and a 3.5 (95% CI = 2.1–6.3) times difference in women, but there was no significant difference in the 5-year risk of sarcopenia between the two highest quartiles (Q3 and Q4). Log-rank testing of Kaplan–Meier plots based upon physical activity quartiles showed significant interquartile differences with respect to the proportion of subjects remaining above the sarcopenia threshold over the 5 years of observation (Figure 1).
tissue mass and age. The Cochran-Armitage test was used to assess trends in loss of lean mass over time for subjects in each physical activity quartile; if trends were significant, the Williams correction was applied when comparing baseline scores with values for Years 1 to 5. Cox proportional hazards regression analysis was used to assess independent relationships between habitual physical activity values and the 5-year risk that lean mass would drop below the sarcopenia threshold, after controlling for baseline lean tissue mass, age, smoking status and alcohol consumption. A Kaplan–Meier plot was used to determine the proportion of subjects in each activity quartile who remained above the sarcopenia threshold in each year of the 5-year follow-up, and log-rank tests were used to analyze the statistical significance of differences in curves between physical activity quartiles. All statistical contrasts were made at the .05 level of significance.
DISCUSSION The present longitudinal study confirms the findings of previous cross-sectional observations:8 older adults with high pedometer/accelerometer scores have greater conservation of lean tissue than individuals who are more sedentary. It further demonstrates that the more-active subjects gain substantial protection against the risk of dropping below a specified sarcopenia threshold over 5 years of follow-up. Nevertheless, a few subjects even in the highest initial quartile of pedometer/accelerometer readings had a lean tissue mass indicative of appendicular sarcopenia at the end of the 5-year study. It remains to be clarified why these individuals were particularly vulnerable to the normal age-related loss of lean tissue, despite having apparently adequate amounts of regular physical activity. Possible explanations include differences of constitution and nutrition, side-effects of medication, and the onset of chronic disease. The body composition data for the longitudinal study were obtained by measuring electrical impedance; with the electrode placement used, the resulting index reflected some 40% of the individual’s total lean tissue mass. In a previous cross-sectional analysis,8 whole-body DXA measurements allowed loss of lean tissue from specific body regions (arm, leg, and combined appendicular sarcopenia) to be distinguished. Some limitations of bioimpedance data have been discussed in an earlier monograph.21 Bioimpedance has less absolute accuracy than DXA, but recent research22,23 shows satisfactory concordance in mean estimates of appendicular mass between the two methods when using the latest types of equipment. Although the prevalence of sarcopenia in the study population was
RESULTS Baseline characteristics showed the anticipated differences in height and body mass between men and women (P < .05); the two groups did not differ significantly with respect to age or body mass index (BMI), but both were substantially shorter than the current generation of North American older adults (Table 1). Moreover, no statistically significant sex differences were observed in the two chosen indices of habitual physical activity: 5-year average daily step count and 5-year average daily duration of exercise at more than 3 METs. As expected, initial lean tissue mass was substantially greater in men than in women. Subjects maintained a surprisingly constant level of physical activity over the 5 years of observation (Table 2). Lean tissue indices were greater for those with higher physical activity scores, more markedly for exercise duration at more than 3 METs than for step count (Table 3), although ANCOVA adjusted for baseline lean tissue mass and age showed no significant difference between the third and fourth activity quartiles. The Cochran-Armitage test showed no significant 5-year loss of lean tissue in either of the two highest activity quartiles (Q3 and Q4). A multivariate-adjusted Cox proportional hazards model predicted that, over the 5-year period of observation, the risk that an individual’s appendicular lean tissue mass would drop below the sarcopenia threshold was much greater for those in the two lowest activity quartiles than for those in the highest quartile (Table 4). In terms of
Table 1. Anthropometric Characteristics, Habitual Physical Activity Patterns, and Appendicular Lean Tissue Mass Indices of Subjects at Entry to Study Characteristic
Age Body mass, kg Height, m Body mass index, kg/m2 Appendicular lean tissue mass, kg/m2 Five-year average step count, steps/d Five-year average duration of physical activity >3 metabolic equivalents, min/d
Men, n = 200
73.5 54.9 1.55 22.8 11.5 6,937 16.8
4.3 10.3 0.21 3.2 2.3 2,312 6.4
Women, n = 268
P-Value for Difference
.43 .004 3 METs Q1 3.8 1.6 Q2 11.3 2.5 Q3 20.2 3.2 Q4 32.0 7.1 Women (n = 67/quartile) Steps per day Q1 3,481 937 Q2 5,703 781 Q3 7,513 713 Q4 10,361 1,621 Min/d of physical activity at >3 METs Q1 3.9 2.0 Q2 10.2 1.9 Q3 16.3 2.2 Q4 30.8 6.9
3
3,719 6,222 7,901 10,931
1,016 883 938 1,610
3.9 11.8 21.2 31.1
1.9 2.1 2.9 6.9
3,791 5,343 7,751 10,251
899 961 691 1,355
3.9 9.9 17.4 32.1
1.8 2.5 2.3 7.8
3,970 6,187 7,689 11,351
1,176 919 903 1,228
4.1 10.8 19.6 33.3
2.0 2.5 2.8 9.8
3,893 5,788 7,726 11,031
991 953 673 1,613
4.0 10.5 17.8 32.9
1.9 2.2 2.1 7.0
4,081 6,128 7,898 10,971
1,131 1,421 927 1,287
4.0 10.0 20.5 32.4
1.9 2.7 3.1 8.8
4,037 5,981 7,931 10,251
1,015 993 851 1,531
4.0 10.9 17.7 32.8
1.5 2.5 2.3 8.4
4,002 6,002 7,923 10,186
1,021 961 794 1,263
4.0 10.5 21.0 31.0
1.9 2.4 3.9 7.7
4,024 5,716 7,556 10,098
1,103 875 788 1,781
4.2 10.9 16.9 30.3
1.9 2.6 2.4 8.1
4,107 5,649 7,600 10,001
1,017 973 924 1,519
.27 .58 .63 .72
3.9 10.4 19.9 30.6
2.0 2.8 4.0 8.2
.21 .57 .77 .64
4,103 5,864 7,683 9,997
1,102 1,021 819 1,462
.19 .53 .66 .71
3.8 11.4 18.0 29.9
1.9 3.6 2.5 7.9
.43 .59 .78 .71
In men, average steps per day: Q1, range 1,294–5,517, 3,899 1,026; Q2, range 5,519–6,731, 6,019 782; Q3, range 6,741–8,978, 7,801 1,052; Q4, range 8,983–16,513, 10,660 1,584 and average min/d of moderate-intensity activity: Q1, range 0.7–7.8, 4.0 1.9; Q2, range 7.9–15.6, 10.9 2.5; Q3, range 15.7–27.9, 20.4 4.1; Q4, range 27.9–70.3, 31.7 11.3. In women, average steps per day: Q1, range 1,360–4,961, 3,887 1,321; Q2, range 4,981–6,841, 5,733 868; Q3, range 6,849–8,331, 7,693 831; Q4, range 8,387–16,918, 10,331 1,671 and average min/d of moderate-intensity activity: Q1, range 0.2–7.9, 4.0 2.3; Q2, range 8.0–14.0, 10.7 2.1; Q3, range 14.1–21.9, 17.4 3.3; Q4, range 22.0–55.8, 31.5 12.9.
similar when based on each of these three statistics, the correlation with pedometer/accelerometer measurements of physical activity was closer for appendicular and leg lean tissue mass than for the arms. Alternatively, a comparison of sarcopenic and nonsarcopenic individuals showed a greater deficiency of lean tissue in the arms (34%) than in the legs (17%). The total volume of lean tissue measured using the DXA method was smaller than that examined using the impedance technique, but the overall conclusions with respect to the benefits of habitual physical activity were similar. The definition of dose-response relationships linking habitual physical activity and some aspect of health such as lower risk of sarcopenia remains challenging. Some authors have postulated that a minimum threshold intensity of activity is needed to obtain any benefit, but others have suggested that the greatest benefit is seen in those who move from a totally sedentary lifestyle to a minimal amount of regular physical activity.24 Much presumably depends upon the population tested; their initial health, fitness, and state of nutrition; and the type of exercise undertaken. Strengths of the present investigation include its longitudinal design, its long duration, and the objective measurement of physical activity, although the study was restricted to one specific community, differing from North America in respect to the sociocultural environment and patterns of medical care. The Japanese subjects were also much shorter and less obese than would be
anticipated in North American seniors, possibly implying lower protein and energy intake over part or all of their lifespan; in such a population, part of the apparent advantage of lean tissue mass seen in an individual with a high level of physical activity could reflect greater food intake than that of his or her peers, with a corresponding greater availability of essential amino acids for synthesis of muscle tissue.25 The pedometer/accelerometer used provides a good objective index of endurance activities such as walking, which was the main source of exercise for most subjects, although the device may be less responsive to resistance exercise, and it is possible that the observed correlations do not reflect the volume of exercise required to protect against sarcopenia. Rather, the study may have identified the more-active members of the community who engage in endurance activity (which as measured) and resistance activity (which the measuring device did not assess). The method used to determine lean body mass and thus sarcopenia (bioimpedance) was appropriate for the number of field assessments required, but it is less precise than some laboratory techniques, does not assess regional lean tissue mass, and reflects only a part of total lean tissue. Moreover, age-related changes in tissue hydration could have influenced the bioimpedance data. A consensus panel meeting in Rome in November 200920 proposed functional criteria of sarcopenia (e.g., being bedridden, being unable to rise independently from a chair, or having
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Table 3. Appendicular Lean Tissue Mass Indices for Initial Visit (Baseline) and for Each of 5 Succeeding Years, Classified According to Quartile (Q1–Q4) of Habitual Physical Activity Baseline
1
2
3
4
5 P-Value for Trend
Mean Standard Deviation
Subject Category
Men (n = 50/quartile) Step count Q1 10.5 2.0 Q2 11.5 1.9 Q3 11.4 2.0 Q4 12.5 1.9 Duration of physical activity at >3 METs Q1 10.3 1.6 Q2 11.1 2.3 Q3 11.8 1.8 Q4 12.7 2.1 Women (n = 67/quartile) Step count Q1 8.0 2.1 Q2 8.8 1.6 Q3 8.9 2.3 Q4 9.5 2.1 Duration of physical activity at >3 METs Q1 7.9 1.8 Q2 8.3 2.1 Q3 9.2 1.8 Q4 9.8 1.7
10.2 11.4 11.3 12.7
2.6 1.3 1.2 1.9
9.9 11.2 11.2 12.4
1.9 1.9 1.8 1.7
9.8 10.9 11.5 12.3
2.8a 1.5a 2.0 2.2
9.7 10.9 10.9 12.3
2.6a 1.4a 1.4 1.7
9.6 10.9 11.0 12.2
2.1a 2.0a 1.9 2.1
.01 .03 .18 .38
10.0 11.0 11.8 12.8
2.6 2.5 2.4 2.4
9.8 10.7 11.7 12.5
2.8 2.1 1.7 1.6
9.6 10.4 11.8 12.7
2.1a 1.8a 1.8 2.4
9.4 10.5 11.5 12.5
2.2a 2.1a 2.1 2.5
9.4 10.3 11.5 12.5
2.4a 2.5a 2.0 1.8
.02 .02 .28 .36
7.8 8.5 8.9 9.5
1.9 2.1 2.6 2.7
7.5 8.4 8.9 9.4
2.0a 2.5 2.6 2.1
7.6 8.3 8.6 9.4
1.9a 2.8 2.9 2.5
7.5 8.2 8.5 9.3
2.0a 2.1a 2.8 2.4
7.4 8.1 8.3 9.3
2.0a 1.9a 2.1 2.7
.03 .02 .17 .13
7.7 8.0 9.1 9.8
2.0 2.1 2.8 2.9
7.4 7.9 9.1 9.7
1.9a 2.1 2.7 3.0
7.3 7.8 9.0 9.7
1.7a 2.1a 2.6 2.7
7.2 7.6 9.0 9.6
1.9a 2.0a 2.3 2.6
7.0 7.6 8.8 9.6
2.1a 1.9a 2.4 2.6
.01 .03 .13 .27
For details of average step counts and average duration of moderate activity in the quartiles, see footnote to Table 2. a Difference from baseline (P < .05). MET = metabolic equivalent.
Table 4. Risk of Appendicular Lean Tissue Mass Index Falling Below the Arbitrary Sarcopenia Threshold over the 5-Year Study, Classified According to Quartile (Q1–Q4) of Habitual Physical Activity (Reference Q4) Men (n = 50/Quartile) Subject Category
Women (n = 67/Quartile)
Relative Risk (95% Confidence Interval)
Step count Q1 2.33 (1.43–4.51) 2.99 Q2 1.97 (1.00–2.86) 2.01 Q3 0.95 (0.43–2.01) 1.03 P-value for trend .04 .03 Duration of physical activity at >3 metabolic equivalents Q1 3.01 (2.02–5.99) 3.49 Q2 1.78 (1.32–4.17) 2.21 Q3 1.13 (0.57–2.15) 0.91 P-value for trend .01 .02
(1.91–3.42) (1.01–3.03) (0.58–2.25)
(2.11–6.32) (1.03–3.61) (0.37–2.51)
Values adjusted for baseline lean tissue mass, age, smoking status, and alcohol intake. For details of average step counts and average duration of moderate activity in the quartiles, see footnote to Table 2.
a measured gait speed of 3 METs) than with volume (daily step count). In this study, individuals in the two most active quartiles of physical activity (≥7,000–8,000 steps/d or ≥15–20 min/d of exercise at an intensity of >3 METs) had a lower probability of losing muscle mass over 5 years than those who were less active. Clinicians should encourage seniors to reach such levels of daily physical activity.
ACKNOWLEDGMENTS This article focuses particularly on data from an interdisciplinary study of the habitual physical activity and health of elderly people living in Nakanojo, Gunma, Japan (the Nakanojo Study). The authors gratefully acknowledge the expert technical assistance of the research and nursing staffs of the Tokyo Metropolitan
Institute of Gerontology, the University of Tokyo, and the Nakanojo Public Health Center. We also thank the subjects whose conscientious participation made the Nakanojo Study possible. Conflict of Interest: This study was supported in part by grants (Grant-in-Aid for Encouragement of Young Scientists 12770037 and Grant-in-Aid for Scientific Research [C]: 15500503, [C]: 17500493, [B]: 19300235, and [B]: 23300259) from the Japan Society for the Promotion of Science. Author Contributions: Roy J. Shephard: interpretation of data, preparation of manuscript. Hyuntae Park: acquisition of subjects and data, analysis of data, preparation of manuscript. Sungjin Park: acquisition of subjects and data. Yukitoshi Aoyagi: study concept and design, acquisition of subjects and data, analysis and interpretation of data, preparation of manuscript. Sponsor’s Role: None.
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