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Geriatr Gerontol Int 2014; 14 (Suppl. 1): 52–60

ORIGINAL ARTICLE

Epidemiology of sarcopenia among community-dwelling older adults in Taiwan: A pooled analysis for a broader adoption of sarcopenia assessments I-Chien Wu,1,2 Cheng-Chieh Lin,2 Chao A. Hsiung,1 Ching-Yi Wang,3 Chih-Hsing Wu,4,5 Ding-Cheng Derrick Chan,6,7 Tsai-Chung Li,8 Wen-Yuan Lin,9 Kuo-Chin Huang,10 Ching-Yu Chen1,10 and Chih-Cheng Hsu1,11 for the Sarcopenia and Translational Aging Research in Taiwan (START) Team* 1

Institute of Population Health Sciences, National Health Research Institutes, Miaoli County, 2Program for Aging, College of Medicine, Graduate Institute of Biostatistics, College of Public Health, China Medical University, 3School of Physical Therapy and Center for Education and Research on Geriatrics and Gerontology, Chung Shan Medical University, 9Department of Family Medicine, China Medical University Hospital, 11Department of Health Services Administration, China Medical University and Hospital, Taichung, 4Department of Family Medicine, National Cheng Kung University Hospital, 5Institute of Gerontology, National Cheng Kung University Medical College, Tainan, Departments of 6Geriatrics and Gerontology and 7Internal Medicine, National Taiwan University Hospital, and 10Department of Family Medicine, College of Medicine, National Taiwan University, Taipei, Taiwan 8

Aim: To develop cut-off points of muscle mass, gait speed and handgrip strength; and to examine the prevalence of sarcopenia, and the relationship between sarcopenia stages and functional limitations and disability by using these cut-off points. Methods: We pooled individual participant data of 2867 community-dwelling older adults from five cohort studies. We defined the cut-off point of a muscle mass index (ASM/ht2) as the values of two standard deviations below the sex-specific means of a young population or as the 20th percentile of the sex-specific distribution in our study population. The gait speed and handgrip strength cut-off points were defined as the 20th percentile of their population distributions. We also measured functional limitations, using the Short Physical Performance Battery, and the number of activities of daily living and instrumental activities of daily living difficulties. Results: We identified the cut-off points of ASM/ht2, gait speed and handgrip strength. By applying these cut-off points to our study population, the prevalence of sarcopenia varied from 3.9% (2.5% in women and 5.4% in men) to 7.3% (6.5% in women and 8.2% in men). A higher sarcopenia stage was independently associated with a lower summary performance score, as well as more activities of daily living and instrumental activities of daily living difficulties (P < 0.05 for all). Conclusions: The prevalence of sarcopenia in community-dwelling older adults is comparable with those in other populations. A dose–response relationship exists between sarcopenia stages and functional limitations/disability. The European Working Group on Sarcopenia in Older People consensus definition using these cut-off points is suitable for determining sarcopenia cases in the elderly population of Taiwan. Geriatr Gerontol Int 2014; 14 (Suppl. 1): 52–60. Keywords: disability evaluation, epidemiology, muscle, physical function, sarcopenia.

Introduction Accepted for publication 5 November 2013. Correspondence: Dr Chih-Cheng Hsu MD DRPH, Institute of Population Health Sciences, National Health Research Institutes, 35 Keyan Road, Zhunan, Miaoli County 35053, Taiwan. Email: [email protected] *Other members of the START Team are listed at the end of this article.

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doi: 10.1111/ggi.12193

The global population is aging, and disabilities later in life are becoming an urgent health issue.1 Skeletal muscles play a critical role in maintaining function later in life.2 However, skeletal muscle mass declines with age.2 Sarcopenia, the age-related loss of skeletal muscle mass and function, is prevalent among older people, and represents a major risk factor of disability, falls, © 2014 Japan Geriatrics Society

Sarcopenia in an elderly population in Taiwan

mortality, and numerous other adverse health outcomes in older adults.2–4 Therefore, the early recognition and diagnosis of sarcopenia in a primary care setting can enable identifying and treating vulnerable older adults at an early stage of the disablement process. Operational definitions and diagnostic criteria have recently been proposed to facilitate the prompt recognition of sarcopenia in clinical practice.3–7 According to the consensus developed by the European Working Group on Sarcopenia in Older People (EWGSOP), the diagnosis of sarcopenia requires the measurement of three variables: muscle mass, physical performance and muscle strength.6 A wide range of assessment techniques with varying costs, availability and ease of use are available for measuring each of these sarcopenia variables.6 Assessment techniques that are economical, readily available, reliable and simple facilitate the widespread adoption of current sarcopenia case-finding strategies in different healthcare settings and large-scale community-based epidemiological studies. Bioelectrical impedance analysis, usual gait speed and handgrip strength are measurement methods used to assess muscle mass, physical performance and muscle strength, respectively, and are extremely promising in this regard.4,6,8,9 Sarcopenia is diagnosed in older adults with low muscle mass plus poor physical performance or muscle strength.6 The EWGSOP also proposed a staging scheme for sarcopenia.6 However, whether the cut-off points of the muscle mass estimate, usual gait speed and handgrip strength determined in Western studies could be applied to other populations with different ethnicities or cultures remains unclear. That racial and ethnic differences in body composition and physical function exist is well known.10–14 The results of previous studies have shown that the proper cut-off points of sarcopenia variables for Asians can differ from those for Westerners.15–23 In the consensus report, the EWGSOP called for the reference values of sarcopenia variables for populations worldwide.6 Because sarcopenia is believed to represent a major cause of disability,6,7 sarcopenia defined using cut-off points should be independently associated with the early indicators of the disablement process, as well as a greater degree of disability among older adults. Specifically, a dose–response relationship should exist between sarcopenia stages, and the indicators of disability risk and severity. To meet the urgent need of defining the subnormal values of muscle mass and physical function for a sarcopenia diagnosis in a rapidly aging Asian population, we pooled primary data from five major cohort studies in Taiwan, as part of the Sarcopenia and Translational Aging Research in Taiwan (START) project. This pooling project, with its large sample, provides a unique opportunity to address issues that cannot be addressed sufficiently in any single study. The purpose © 2014 Japan Geriatrics Society

of the present study was to develop muscle mass, gait speed and handgrip strength cut-off points based on population distributions, which were then used in the EWGSOP diagnostic criteria of sarcopenia to determine its prevalence and relationship with functional health in a large sample of community-dwelling older adults in Taiwan.

Methods Participants We analyzed the individual participant data of 2867 community-dwelling older adults, which were collected during baseline examinations of five cohort studies carried out between 2003 and 2012 (Table 1). Details of the designs and participant recruitment of these studies have been published previously.24–26 All of the cohort studies required written informed consent, and were approved by the respective institutional review boards.

Body composition Body composition was measured using an 8-contact electrode bioelectrical impedance analysis (BIA) device (Tanita BC-418, Tanita, Tokyo, Japan), and followed the standard procedure and the manufacturer’s instructions.27 This BIA device was used to measure the wholebody and segmental impedance (± 1Ω) at a frequency of 50 kHz, and it provided valid muscle mass estimates (kg) of each of the four extremities.8 Appendicular muscle mass (ASM) was calculated as the sum of the estimated muscle mass for the arms and legs. A relative skeletal muscle mass index (ASM/ht2) normalized for height was defined as the ratio of ASM (kg) and the height squared (m2).4,6 For this analysis, we defined muscle mass cut-off points according to the distribution of ASM/ht2 of a young population comprising 998 healthy adults (aged 20–40 years)16 or the study population. A participant was considered to have low muscle mass if his or her ASM/ht2 was below −2 standard deviations of the reference young adult values defined in previous studies (6.76 kg/m2 for men and 5.28 kg/m2 for women).16 Alternatively, based on the definition by Delmonico et al. and Newman et al.3,5 we examined the sex-specific distribution of ASM/ht2 in our study population, and participants with ASM/ht2 in the lowest 20% of the sex-specific distribution were considered to have low muscle mass.

Gait speed Participants were observed taking a walk over a short distance at their usual pace, starting from a standing position, and an examiner timed the task by using a |

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(8.5) (8.0) (8.2) (8.3) (8.0) (10.5) (10.4) (9.6) (10.6) (10.8) 61.1 60.9 61.7 62.5 58.8 43.6 51.9 55.9 46.6 51.9 73.4 74.2 74.3 74.5 76.0 2012 2009 2003 2008 2012 Taipei, Kaohsiung Taichung Hualien Taichung Kaohsiung HALST TCHS-E IPFCEH COMDLST TOP

Community Community Community Community Community

713 1042 340 223 549

(%)

COMDLST, Community-dwelling Older Adult’s Mobility Disability Longitudinal Follow Up Study in Taichung City–Development of a Mobility Disability Screening Tool and Plan; HALST, Healthy Aging Longitudinal Study in Taiwan; IPFCEH, Investigation of Physical Function Status of Community Elderly Adults in Hualien city; TCHS-E, Taichung Community Health Study-Elders; TOP, Tianliao Old People Study.

24.4 24.4 24.4 24.9 24.4 158.2 157.8 159.0 158.4 154.9

(3.4) (3.6) (3.2) (3.5) (3.8)

Mean (SD) body mass index (kg/m2) Mean age at entry (years) Year of starting enrolment No. participants n Setting Study location Study

Table 1 Characteristics of the cohort studies included in the pooled analysis†

Men

Mean (SD) weight (kg)

Mean (SD) height (cm)

I-C Wu et al.

handheld stopwatch that measured to the nearest hundredth of a second. The walking distance ranged from 3 to 5 m according to different study sites. The gait speed was calculated as the walking distance (m) divided by time (s). We examined the distribution of the gait speed stratified according to the sex-specific median height. Participants with a gait speed in the lowest 20% of the sex- and height-specific distributions were considered to have low gait speed.6,28

Handgrip strength Handgrip strength (kg) was measured using standard calibrated hand dynamometers.24,25 We calculated the average grip strength of each hand, and the average grip strength of the hand with superior performance or that of the dominant hand was used for the analysis. We examined the distribution of the handgrip strength stratified according to sex-specific body mass index (BMI) quartiles. Participants with a handgrip strength in the lowest 20% of the sex- and BMI-specific distributions were considered to have low handgrip strength.6,28

Sarcopenia We determined the presence of sarcopenia according to the EWGSOP consensus definition.6 A diagnosis of sarcopenia requires the presence of low muscle mass in addition to a low handgrip strength or a slow gait speed. Participants were considered to have severe sarcopenia if all three of these criteria were present, whereas those with low muscle mass, but without a low handgrip strength or a slow gait speed, were considered to be in the presarcopenia stage.

Functional health status We assessed functional limitations by using the Short Physical Performance Battery (SPPB).29 A participant received a summary performance score on this scale, with a higher score representing better performance. A lower summary performance score predicts disability in a linear fashion across the entire range of values.29 We also assessed the perceived function in the activities of daily living (ADL) and the instrumental activities of daily living (IADL) by carrying out structured interviews with the Katz Index, the Barthel Index and the Lawton–Brody Instrumental Activities of Daily Living Scale, which evaluate the level of dependence in carrying out each task.30–32 The severity of a disability was defined using the number of ADL (i.e. eating, transferring, personal hygiene, bathing, walking, dressing and continence) and IADL (i.e. shopping, housekeeping, handling finances, food preparation, using transportation, using a telephone, doing the laundry and taking medication) that the person was unable to carry out independently.33 © 2014 Japan Geriatrics Society

Sarcopenia in an elderly population in Taiwan

Covariates The covariates were the participant’s age, sex, education level (≤6 years or >6 years), smoking status (smoker or non-smoker), obesity status and comorbidities. Participants who reported smoking cigarettes at the time of the interview were defined as smokers. We calculated the BMI as the bodyweight in kg divided by the square of the height in m2, and categorized it according to the definition of the Department of Health in Taiwan (BMI 24–26.9 kg/m2 for overweight and BMI ≥27 kg/m2 for obesity).34 Comorbidities were assessed by referring to the self-reported physician’s diagnosis, and included hypertension, diabetes mellitus, stroke, heart disease, arthritis, and chronic obstructive pulmonary disease.

Statistical analysis Descriptive statistics were used to characterize the population. All of the continuous variables are presented as the mean ± SD. Differences in continuous variables among the groups were analyzed using oneway analysis of variance (ANOVA), whereas differences in categorical variables (proportions) were analyzed using χ2-tests. We examined the relationship between the sarcopenia severity/stage and the functional health measures by applying linear regression analysis. We included the following covariates in the adjusted model: age, sex, education level, smoking status, obesity status, comorbidities and cohorts. We estimated the adjusted values of the summary performance score, and the number of ADL and IADL difficulties according to the sarcopenia severity/stages. In all of the analyses, differences were considered significant when P < 0.05. We calculated 95% confidence intervals (CI), and reported the CI for each parameter estimate. All of the analyses were carried out using SPSS version 19.0 (SPSS, Chicago, IL, USA).

Results The mean ± SD value of the participants’ age was 74 ± 6 years, and 50% of the participants were women. The mean ± SD values of the sarcopenia variables were as follows: ASM/ht2, 6.38 ± 0.82 kg/m2 in women, and 8.05 ± 1.15 kg/m2 in men; gait speed, 0.82 ± 0.26 m/s in women, and 0.90 ± 0.27 m/s in men; and handgrip strength, 20.0 ± 5.4 kg in women, and 32.3 ± 7.4 kg in men. The cut-off points for low muscle mass, low physical performance and low muscle strength are summarized in Table 2. After applying the EWGSOP diagnostic criteria of sarcopenia with muscle mass cut-off points derived from reference young adults, we observed a prevalence of sarcopenia of 2.5% among women and 5.4% among © 2014 Japan Geriatrics Society

Table 2 Cut-off points of the sarcopenia variables Cut-off points Muscle mass (ASM/ht2) Men Women Physical performance (gait speed)§ Men Height ≤163 cm Height >163 cm Women Height ≤152 cm Height >152 cm Muscle strength (handgrip strength)¶ Men BMI 26.3 kg/m2 Women BMI 26.8 kg/m2

6.76 kg/m2† 7.09 kg/m2‡ 5.28 kg/m2† 5.70 kg/m2‡

0.67 m/s 0.71 m/s 0.57 m/s 0.67 m/s

25.0 kg 26.5 kg 26.4 kg 27.2 kg 14.6 kg 16.1 kg 16.5 kg 16.4 kg

† Defined as values two standard deviations below the sex-specific means of the reference young adults aged 20–40 years. ‡Defined as the 20th percentile of the sex-specific distribution in our study population. §Defined as the 20th percentile of the sex- and height-specific distribution in our study population. ¶Defined as the 20th percentile of the sexand body mass index (BMI)-specific distribution in our study population. ASM, appendicular muscle mass.

men. The corresponding values were 6.5% in women and 8.2% in men when using the muscle mass cut-off points derived from the study population. As expected, the prevalence of sarcopenia increased significantly with age in both sexes (Table 3). Participants with sarcopenia were more likely to be older, lean and diagnosed with a chronic disease (Table 4). Older adults at a more advanced stage of sarcopenia tended to have a lower summary performance score as well as difficulties in more ADL and IADL (Table 4). After adjusting for covariates, the increasing sarcopenia level remained significantly associated with a lower summary performance score, and more ADL and IADL difficulties (Table 5). Using muscle mass cut-off points derived from the reference young adults, we found that participants with severe sarcopenia had a mean of 1.42 more ADL difficulties (P < 0.001), a mean of 1.54 more IADL difficulties (P < 0.001), and their summary performance score was a mean of 2.5 points lower (P = 0.042) compared with |

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Low muscle mass only. ‡Low muscle mass + slower walking speed or low muscle mass + low handgrip strength. §Low muscle mass + slower walking speed + low handgrip strength. ¶Sarcopenia + severe sarcopenia. †

354 (74.1) 59 (12.3) 36 (7.5) 29 (6.1) 65 (13.6) 496 (86.0) 60 (10.4) 19 (3.3) 2 (0.3) 21 (3.6) 340 (78.2) 49 (11.3) 28 (4.6) 18 (4.1) 46 (10.6) Muscle mass cut-off points derived from the study population No sarcopenia 1732 (80.4) 882 (80.2) 542 (81.5) † 266 (12.3) 147 (13.4) 98 (14.7) Presarcopenia ‡ 105 (4.9) 50 (4.5) 22 (3.3) Sarcopenia § 52 (2.4) 21 (1.9) 3 (0.5) Severe sarcopenia ¶ 157 (7.3) 71 (6.5) 25 (3.8) Any sarcopenia

850 (80.6) 119 (11.3) 55 (5.2) 31 (2.9) 86 (8.2)

406 (84.9) 27 (5.6) 23 (4.8) 22 (4.6) 45 (9.4) 535 (92.7) 30 (5.2) 10 (1.7) 2 (0.3) 12 (2.1) 941 (89.2) 57 (5.4) 33 (3.1) 24 (2.3) 57 (5.4) 394 (90.6) 20 (4.6) 11 (2.5) 10 (2.3) 21 (4.8)

n (%)

Muscle mass cut-off points derived from reference young population No sarcopenia 1964 (91.1) 1023 (93.0) 629 (94.6) † 106 (4.9) 49 (4.5) 29 (4.4) Presarcopenia ‡ 50 (2.3) 17 (1.5) 6 (0.9) Sarcopenia § 35 (1.6) 11 (1.0) 1 (0.2) Severe sarcopenia ¶ 85 (3.9) 28 (2.5) 7 (1.1) Any sarcopenia

Men All ages n (%) Aged ≥75 years n (%) Aged 65–74 years n (%) Women All ages n (%) All

Table 3 Prevalence of sarcopenia using European Working Group on Sarcopenia in Older People definitions

Aged 65–74 years n (%)

Aged ≥75 years n (%)

I-C Wu et al.

those without sarcopenia. We observed a similar pattern when using the muscle mass cut-off points derived from the study population (Table 5).

Discussion In the present pooled analysis of five cohort studies, we identified the cut-off points of a relative skeletal muscle mass index, usual gait speed and handgrip strength, based on the population distributions. The prevalence of sarcopenia among community-dwelling older adults was also estimated. Based on the staging scheme proposed by the EWGSOP, the sarcopenia severity/stage was found to be related to degrees of functional limitations and disabilities in a dose–response manner, independent of potential confounders. The ASM/ht2 cut-off points derived from our reference young population were 6.76 kg/m2 for men and 5.28 kg/m2 for women, which are values similar to those in a Japanese population (6.87 kg/m2 for men and 5.46 kg/m2 for women),23 although they were slightly higher than those in a South Korean population (6.58 kg/m2 for men and 4.59 kg/m2 for women)19 and a Chinese population (6.08 kg/m2 for men and 4.79 kg/m2 for women).17 Slight variations in muscle mass distributions among young adults might be owing to differences in early life determinants of peak muscle mass.35 The use of muscle mass cut-off points derived from healthy young adults is recommended; however, researchers have suggested alternative methods of defining subnormal muscle mass.3,5,6 The ASM/ht2 values of 7.09 kg/m2 in men and 5.70 kg/m2 in women corresponded to the 20th percentile of the sex-specific distribution in our study population. These values are similar to the ASM/ ht2 values identified in other populations comprising older adults.3,5 Newman et al. noted that the ASM/ht2 values of 7.23 kg/m2 in men and 5.67 kg/m2 in women represented the 20th percentile values in a USA population of older adults aged 70 years and older.5 In general, the muscle mass cut-off points indentified in the present study were congruent with previous studies’ findings. The mean gait speed in the present study was 0.90 ± 0.27 m/s in men and 0.82 ± 0.26 m/s in women. This is in agreement with the results of studies that had recruited elderly Chinese cohort populations.12 However, these estimates were lower than those observed in Western populations.36,37 In a study that recruited 1750 community-dwelling Caucasian older adults aged 70 years and older, men had a mean gait speed of 1.15 m/s, and women had a mean gait speed of 1.08 m/s.37 The racial/ethnic differences in gait speed values could partly be due to differences in anthropometrics.11 Because gait speed is known to differ significantly based on a person’s sex and height,36,37 we examined the distributions according to the sex-specific © 2014 Japan Geriatrics Society

Sarcopenia in an elderly population in Taiwan

Table 4 Characteristics of study participants according to sarcopenia status (n = 2155)† Characteristics

No sarcopenia

Presarcopenia‡

Sarcopenia§

Severe sarcopenia¶

P

78.6 (7.3) 33 (66.0)

81.7 (6.2) 24 (68.6)

Epidemiology of sarcopenia among community-dwelling older adults in Taiwan: a pooled analysis for a broader adoption of sarcopenia assessments.

To develop cut-off points of muscle mass, gait speed and handgrip strength; and to examine the prevalence of sarcopenia, and the relationship between ...
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