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O R I G I N A L A R T I C L E

Epidemiology of sarcopenia among community-dwellingolder adults in Taiwan: A pooled analysis for a broaderadoption 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*

1Institute of Population Health Sciences, National Health Research Institutes, Miaoli County, 2Program for Aging, College of Medicine,8Graduate 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 of6Geriatrics and Gerontology and 7Internal Medicine, National Taiwan University Hospital, and10Department of

Family Medicine, College of Medicine, National Taiwan University, Taipei, Taiwan

Aim: To develop cut-off points of muscle mass, gait speed and handgrip strength; and to examine the prevalenceof sarcopenia, and the relationship between sarcopenia stages and functional limitations and disability by using thesecut-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 thesex-specific means of a young population or as the 20th percentile of the sex-specific distribution in our studypopulation. The gait speed and handgrip strength cut-off points were defined as the 20th percentile of theirpopulation distributions. We also measured functional limitations, using the Short Physical Performance Battery, andthe 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-offpoints 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 lowersummary performance score, as well as more activities of daily living and instrumental activities of daily livingdifficulties (P< 0.05 for all).

Conclusions: The prevalence of sarcopenia in community-dwelling older adults is comparable with those in otherpopulations. A doseresponse relationship exists between sarcopenia stages and functional limitations/disability. TheEuropean Working Group on Sarcopenia in Older People consensus definition using these cut-off points is suitablefor determining sarcopenia cases in the elderly population of Taiwan. Geriatr Gerontol Int 2014; 14 (Suppl. 1):5260.

Keywords:disability evaluation, epidemiology, muscle, physical function, sarcopenia.

Introduction

The global population is aging, and disabilities later inlife are becoming an urgent health issue.1 Skeletalmuscles play a critical role in maintaining function laterin life.2 However, skeletal muscle mass declines withage.2 Sarcopenia, the age-related loss of skeletal musclemass and function, is prevalent among older people,and represents a major risk factor of disability, falls,

Accepted for publication 5 November 2013.

Correspondence: Dr Chih-Cheng Hsu MD DRPH, Institute ofPopulation Health Sciences, National Health ResearchInstitutes, 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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Geriatr Gerontol Int 2014; 14 (Suppl. 1): 5260

52 | 2014 Japan Geriatrics Societydoi: 10.1111/ggi.12193
mailto:[email protected]:[email protected]


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mortality, and numerous other adverse health outcomesin older adults.24 Therefore, the early recognition anddiagnosis of sarcopenia in a primary care setting canenable identifying and treating vulnerable older adults atan early stage of the disablement process.

Operational definitions and diagnostic criteria have

recently been proposed to facilitate the prompt recog-nition of sarcopenia in clinical practice.37 According tothe consensus developed by the European WorkingGroup on Sarcopenia in Older People (EWGSOP), thediagnosis of sarcopenia requires the measurement ofthree variables: muscle mass, physical performance andmuscle strength.6 A wide range of assessment tech-niques with varying costs, availability and ease of use areavailable for measuring each of these sarcopenia vari-ables.6 Assessment techniques that are economical,readily available, reliable and simple facilitate the wide-spread adoption of current sarcopenia case-finding

strategies in different healthcare settings and large-scalecommunity-based epidemiological studies. Bioelectricalimpedance analysis, usual gait speed and handgripstrength are measurement methods used to assessmuscle mass, physical performance and musclestrength, respectively, and are extremely promising inthis regard.4,6,8,9

Sarcopenia is diagnosed in older adults with lowmuscle mass plus poor physical performance or musclestrength.6 The EWGSOP also proposed a stagingscheme for sarcopenia.6 However, whether the cut-offpoints of the muscle mass estimate, usual gait speed andhandgrip strength determined in Western studies couldbe applied to other populations with different ethnicitiesor cultures remains unclear. That racial and ethnic dif-ferences in body composition and physical functionexist is well known.1014 The results of previous studieshave shown that the proper cut-off points of sarco-penia variables for Asians can differ from those forWesterners.1523 In the consensus report, the EWGSOPcalled for the reference values of sarcopenia variables forpopulations worldwide.6 Because sarcopenia is believedto represent a major cause of disability,6,7 sarcopeniadefined using cut-off points should be independentlyassociated with the early indicators of the disablement

process, as well as a greater degree of disability amongolder adults. Specifically, a doseresponse relationshipshould exist between sarcopenia stages, and the indica-tors of disability risk and severity.

To meet the urgent need of defining the subnormalvalues of muscle mass and physical function for asarcopenia diagnosis in a rapidly aging Asian popula-tion, we pooled primary data from five major cohortstudies in Taiwan, as part of the Sarcopenia and Trans-lational Aging Research in Taiwan (START) project.This pooling project, with its large sample, provides aunique opportunity to address issues that cannot be

addressed sufficiently in any single study. The purpose

of the present study was to develop muscle mass, gaitspeed and handgrip strength cut-off points based onpopulation distributions, which were then used in theEWGSOP diagnostic criteria of sarcopenia to determineits prevalence and relationship with functional health ina large sample of community-dwelling older adults in

Taiwan.

Methods

Participants

We analyzed the individual participant data of 2867community-dwelling older adults, which were collectedduring baseline examinations of five cohort studiescarried out between 2003 and 2012 (Table 1). Details ofthe designs and participant recruitment of these studieshave been published previously.2426 All of the cohort

studies required written informed consent, and wereapproved by the respective institutional review boards.

Body composition

Body composition was measured using an 8-contactelectrode bioelectrical impedance analysis (BIA) device(Tanita BC-418, Tanita, Tokyo, Japan), and followedthe standard procedure and the manufacturers instruc-tions.27 This BIA device was used to measure the whole-body and segmental impedance (1) at a frequency of50 kHz, and it provided valid muscle mass estimates (kg)of each of the four extremities.8 Appendicular musclemass (ASM) was calculated as the sum of the estimatedmuscle mass for the arms and legs. A relative skeletalmuscle mass index (ASM/ht2) normalized for height wasdefined as the ratio of ASM (kg) and the height squared(m2).4,6

For this analysis, we defined muscle mass cut-offpoints according to the distribution of ASM/ht2 of ayoung population comprising 998 healthy adults (aged2040 years)16 or the study population. A participantwas considered to have low muscle mass if his or herASM/ht2 was below2 standard deviations of the refer-ence young adult values defined in previous studies

(6.76 kg/m2 for men and 5.28 kg/m2 for women).16Alternatively, based on the definition by Delmonicoet al. and Newman et al.3,5 we examined the sex-specificdistribution of ASM/ht2 in our study population, andparticipants with ASM/ht2 in the lowest 20% of thesex-specific distribution were considered to have lowmuscle mass.

Gait speed

Participants were observed taking a walk over a shortdistance at their usual pace, starting from a standing

position, and an examiner timed the task by using a

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handheld stopwatch that measured to the nearest hun-dredth of a second. The walking distance ranged from 3to 5 m according to different study sites. The gait speedwas calculated as the walking distance (m) divided bytime (s). We examined the distribution of the gait speedstratified according to the sex-specific median height.

Participants with a gait speed in the lowest 20% of thesex- and height-specific distributions were consideredto have low gait speed.6,28

Handgrip strength

Handgrip strength (kg) was measured using standardcalibrated hand dynamometers.24,25 We calculated theaverage grip strength of each hand, and the average gripstrength of the hand with superior performance or thatof the dominant hand was used for the analysis. Weexamined the distribution of the handgrip strength

stratified according to sex-specific body mass index(BMI) quartiles. Participants with a handgrip strength inthe lowest 20% of the sex- and BMI-specific distribu-tions were considered to have low handgrip strength.6,28

Sarcopenia

We determined the presence of sarcopenia accordingto the EWGSOP consensus definition.6 A diagnosis ofsarcopenia requires the presence of low muscle mass inaddition to a low handgrip strength or a slow gait speed.Participants were considered to have severe sarcopeniaif all three of these criteria were present, whereas thosewith low muscle mass, but without a low handgripstrength or a slow gait speed, were considered to be inthe presarcopenia stage.

Functional health status

We assessed functional limitations by using the ShortPhysical Performance Battery (SPPB).29 A participantreceived a summary performance score on this scale,with a higher score representing better performance. Alower summary performance score predicts disability ina linear fashion across the entire range of values. 29 We

also assessed the perceived function in the activities ofdaily living (ADL) and the instrumental activities of dailyliving (IADL) by carrying out structured interviews withthe Katz Index, the Barthel Index and the LawtonBrodyInstrumental Activities of Daily Living Scale, whichevaluate the level of dependence in carrying out eachtask.3032 The severity of a disability was defined usingthe number of ADL (i.e. eating, transferring, personalhygiene, bathing, walking, dressing and continence) andIADL (i.e. shopping, housekeeping, handling finances,food preparation, using transportation, using a tele-phone, doing the laundry and taking medication) that

the person was unable to carry out independently.

33Table1

Characteristicsofthecohortstudiesincludedinthepooled

analysis

Study

Studylocation

Setting

No.participants

Y

earofstarting

e

nrolment

Meanage

atentry

Me

n

Mean(SD)

weight

Mean(SD)

height

Mean(SD)body

massindex

n

(years)

(%)

(kg)

(cm)

(kg/m2)

HALST

Taipei,Kaohsiung

Community

713

2

012

73.4

43.6

61.1(10.5)

158.2(8.5)

24.4(3.4)

TCHS-E

Taichung

Community

1042

2

009

74.2

51.9

60.9(10.4)

157.8(8.0)

24.4(3.6)

IPFCEH

Hualien

Community

340

2

003

74.3

55.9

61.7(9.6)

159.0(8.2)

24.4(3.2)

COMDLST

Taichung

Community

223

2

008

74.5

46.6

62.5(10.6)

158.4(8.3)

24.9(3.5)

TOP

Kaohsiung

Community

549

2

012

76.0

51.9

58.8(10.8)

154.9(8.0)

24.4(3.8)

COMDLST,Community-dwellingOld

erAdultsMobilityDisabilityLongitud

inalFollowUpStudyinTaichungCityDevelopmentofaMobilityDisabilityScreeningTool

andPlan;HALST,HealthyAgingLongitudinalStudyinTaiwan;IPFCEH,In

vestigationofPhysicalFunctionStatusofCommunityElderlyAdultsinHualiencity;

TCHS-E,TaichungCommunityHealthStudy-Elders;TOP,TianliaoOldPeopleStudy.

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Covariates

The covariates were the participants age, sex, educationlevel (6 years or >6 years), smoking status (smoker ornon-smoker), obesity status and comorbidities. Partici-pants who reported smoking cigarettes at the time of the

interview were defined as smokers. We calculated theBMI as the bodyweight in kg divided by the square ofthe height in m2, and categorized it according to thedefinition of the Department of Health in Taiwan (BMI2426.9 kg/m2 for overweight and BMI 27 kg/m2 forobesity).34 Comorbidities were assessed by referring tothe self-reported physicians diagnosis, and includedhypertension, 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 pre-sented as the mean SD. Differences in continuousvariables among the groups were analyzed using one-way analysis of variance (ANOVA), whereas differences incategorical variables (proportions) were analyzed using2-tests.

We examined the relationship between the sarcopeniaseverity/stage and the functional health measures byapplying linear regression analysis. We included thefollowing 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 thenumber of ADL and IADL difficulties according to thesarcopenia severity/stages. In all of the analyses, differ-ences were considered significant when P< 0.05. Wecalculated 95% confidence intervals (CI), and reportedthe CI for each parameter estimate. All of the analyseswere 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. Themean SD values of the sarcopenia variables were asfollows: ASM/ht2, 6.38 0.82 kg/m2 in women, and8.05 1.15 kg/m2 in men; gait speed, 0.82 0.26 m/s inwomen, and 0.90 0.27 m/s in men; and handgripstrength, 20.0 5.4 kg in women, and 32.3 7.4 kg inmen. The cut-off points for low muscle mass, lowphysical performance and low muscle strength are sum-marized in Table 2.

After applying the EWGSOP diagnostic criteria ofsarcopenia with muscle mass cut-off points derivedfrom reference young adults, we observed a prevalence

of sarcopenia of 2.5% among women and 5.4% among

men. The corresponding values were 6.5% in womenand 8.2% in men when using the muscle mass cut-offpoints derived from the study population. As expected,the prevalence of sarcopenia increased significantly withage in both sexes (Table 3).

Participants with sarcopenia were more likely to beolder, lean and diagnosed with a chronic disease

(Table 4). Older adults at a more advanced stage ofsarcopenia tended to have a lower summary perfor-mance score as well as difficulties in more ADL andIADL (Table 4). After adjusting for covariates, theincreasing sarcopenia level remained significantly asso-ciated with a lower summary performance score, andmore ADL and IADL difficulties (Table 5). Usingmuscle mass cut-off points derived from the referenceyoung adults, we found that participants with severesarcopenia 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

Table 2 Cut-off points of the sarcopenia variables

Cut-off points

Muscle mass (ASM/ht2)Men 6.76 kg/m2

7.09 kg/m2

Women 5.28 kg/m2

5.70 kg/m2

Physical performance (gait speed)

MenHeight163 cm 0.67 m/sHeight>163 cm 0.71 m/s

WomenHeight152 cm 0.57 m/sHeight>152 cm 0.67 m/s

Muscle strength (handgrip strength)

MenBMI26.3 kg/m2 27.2 kg

WomenBMI26.8 kg/m2 16.4 kg

Defined as values two standard deviations below thesex-specific means of the reference young adults aged 2040

years. Defined as the 20th percentile of the sex-specificdistribution in our study population. Defined as the 20thpercentile of the sex- and height-specific distribution in our

study population. Defined as the 20th percentile of the sex-and body mass index (BMI)-specific distribution in our studypopulation. ASM, appendicular muscle mass.

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2014 Japan Geriatrics Society | 55


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

Discussion

In the present pooled analysis of five cohort studies, weidentified the cut-off points of a relative skeletal musclemass index, usual gait speed and handgrip strength,based on the population distributions. The prevalenceof sarcopenia among community-dwelling older adultswas also estimated. Based on the staging scheme pro-posed by the EWGSOP, the sarcopenia severity/stagewas found to be related to degrees of functional limita-tions and disabilities in a doseresponse manner, inde-pendent of potential confounders.

The ASM/ht2 cut-off points derived from our refer-ence young population were 6.76 kg/m2 for men and

5.28 kg/m2

for women, which are values similar to thosein a Japanese population (6.87 kg/m2 for men and5.46 kg/m2 for women),23 although they were slightlyhigher than those in a South Korean population(6.58 kg/m2 for men and 4.59 kg/m2 for women)19 and aChinese population (6.08 kg/m2 for men and 4.79 kg/m2

for women).17 Slight variations in muscle mass distribu-tions among young adults might be owing to differencesin early life determinants of peak muscle mass.35 Theuse of muscle mass cut-off points derived from healthyyoung adults is recommended; however, researchershave suggested alternative methods of defining subnor-mal 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 the20th percentile of the sex-specific distribution in ourstudy population. These values are similar to the ASM/ht2 values identified in other populations comprisingolder 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 womenrepresented the 20th percentile values in a USA popu-lation of older adults aged 70 years and older.5 Ingeneral, the muscle mass cut-off points indentified inthe present study were congruent with previous studiesfindings.

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 thathad recruited elderly Chinese cohort populations.12

However, these estimates were lower than thoseobserved in Western populations.36,37 In a study thatrecruited 1750 community-dwelling Caucasian olderadults aged 70 years and older, men had a mean gaitspeed of 1.15 m/s, and women had a mean gait speedof 1.08 m/s.37 The racial/ethnic differences in gaitspeed values could partly be due to differences inanthropometrics.11 Because gait speed is known to differsignificantly based on a persons sex and height,36,37 we

examined the distributions according to the sex-specificTable3

Prevalenceofsarcopenia

usingEuropeanWorkingGroupo

nSarcopeniainOlderPeopledefinitions

All

Women

Men

Allages

Aged6574

years

Aged75years

Allages

Aged6574years

Aged75years

n

(%)

n

(%)

n

(%)

n

(%)

n(%)

n

(%)

n

(%)

Musclemasscut-offpointsderived

fromreferenceyoungpopulation

Nosarcopenia

1964(91.1)

1023(93.0)

629(94.6)

394(90.6)

941(89.2)

535(92.7)

406(84.9)

Presarcopenia

106(4.9)

49(4.5)

29(4.4)

20(4.6)

57(5.4)

30(5.2)

27(5.6)

Sarcopenia

50(2.3)

17(1.5)

6(0.9)

11(2.5)

33(3.1)

10(1.7)

23(4.8)

Severesarcopenia

35(1.6)

11(1.0)

1(0.2)

10(2.3)

24(2.3)

2(0.3)

22(4.6)

Anysarcopenia

85(3.9)

28(2.5)

7(1.1)

21(4.8)

57(5.4)

12(2.1)

45(9.4)


fromthestudypopulation

Nosarcopenia

1732(80.4)

882(80.2)

542(81.5)

340(78.2)

850(80.6)

496(86.0)

354(74.1)

Presarcopenia

266(12.3)

147(13.4)

98(14.7)

49(11.3)

119(11.3)

60(10.4)

59(12.3)

Sarcopenia

105(4.9)

50(4.5)

22(3.3)

28(4.6)

55(5.2)

19(3.3)

36(7.5)

Severesarcopenia

52(2.4)

21(1.9)

3(0.5)

18(4.1)

31(2.9)

2(0.3)

29(6.1)

Anysarcopenia

157(7.3)

71(6.5)

25(3.8)

46(10.6)

86(8.2)

21(3.6)

65(13.6)

Lowmusclemassonly.

Lowmusclemass+slowerwalkingspeedorlowmusclemass+lowhandgripstrength.

Lowmusclemass+slowerwalkingspeed+lowhandgrip

strength.

Sarcopenia+severesarcopen

ia.

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median height. As expected, the gait speed cut-offpoints corresponding to the 20th percentile of the dis-tributions were typically lower than those identified inWestern populations,6,28 further emphasizing the needfor ethnicity- or population-specific norms for physical

performance measures.

In the present study, older Taiwanese men had amean handgrip strength of 32.3 7.4 kg, and womenhad a mean handgrip strength of 20.0 5.4 kg. Bothvalues were lower than those observed in Westernpopulations.13,14 This is consistent with the findings

from other Asian populations.

38

To account for the

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

Characteristics No sarcopenia Presarcopenia Sarcopenia Severesarcopenia

P

Muscle mass cut-off points derived from reference young populationAge (years) 74.0 (6.0) 74.3 (6.4) 78.6 (7.3) 81.7 (6.2)


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effects of sex and BMI,13,39 the handgrip strength distri-butions were stratified according to the sex-specific BMIquartiles, and we identified the 20th percentile of thedistribution in each stratum as the handgrip strengthcut-off point. Similarly to the gait speed, the handgripstrength cut-off points identified in the present study

were lower compared with those obtained in Westernstudies.6,28

According to the EWGSOP consensus definition, theprevalence of sarcopenia in our study population variedfrom 3.9% when using muscle mass cut-off pointsderived from a young population to 7.3% when usingmuscle mass cut-off points derived from our largesample of community-dwelling older adults. In addi-tion, the sarcopenia prevalence increased with age, withthe prevalence reaching 13.6% among older men aged75 years and older. These findings are congruent withthe results of recent studies that have applied the

EWGSOP operational definition of sarcopenia in differ-ent populations. Lee et al. noted a prevalence of 7.8%in a sample of 408 elderly Taiwanese participants aged65 years and older.15 In an elderly UK populationwith a mean age of 67 years, 4.6% of men and 7.9% ofwomen were found to have sarcopenia.40 A recent studyobserved a prevalence of 5% in a USA population aged7079 years.41 Legrandet al. showed that the prevalenceof sarcopenia was 12.5% in a European population aged80 years and older.42

Our study showed that the sarcopenia severity/stageis independently associated with the summary perfor-mance score, and the number of ADL and IADL diffi-culties. Older adults with a higher stage of sarcopeniatended to have a lower summary performance score,and more ADL and IADL difficulties. The observeddoseresponse relationship between the sarcopeniastages, and the indicators of disability risk and severitysuggested a gradient of an increasing risk of disabilitydevelopment and progression through these stages.These results are in agreement with the working defi-nition of sarcopenia, as well as the current understand-ing of its progression.6,41

The present study has a number of strengths. Weused a large sample of individual participant data from

multiple diverse populations of community-dwellingolder adults in this pooled analysis. We used techniquesthat are simple, economical, and practical for measuringmuscle mass, muscle strength, and physical perfor-mance. This study is one of the few attempts to definethe cut-off points of all three sarcopenia variables, esti-mate the prevalence of sarcopenia in a rapidly agingAsian population in accordance with the consensusdeveloped by the EWGSOP, and examine the relation-ship between the sarcopenia stages and the functionalhealth measures. Despite these strengths, the presentresults should be interpreted with caution because of

several potential limitations. This was a cross-sectionalTable5

Multivariateanalysestestingassociationsofsarcopeniastag

eswithfunctionalhealthstatus

SarcopeniaStages

Differencebetween

severesarcopenia

andnosarcopenia

95%CI

P

fortrend

N

osarcopenia

Presarcopenia

Sarcopenia

Severe

sarcopenia


fromreferenceyoungpopulation

Summaryperformancescore

10.1

10.6

9.7

7.6

2.5

4.96,0.09

0.042

No.ADLdifficulties

0.13

0.06

0.14

1.55

1.42

1.23,1.62

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