Comparisons of predictive values of sarcopenia with different muscle mass indices in Korean rural older adults: a longitudinal analysis of the Aging Study of PyeongChang Rural Area
Clinical Interventions in Aging
Comparisons of predictive values of sarcopenia with different muscle mass indices in Korean rural older adults: a longitudinal analysis of the Aging study of PyeongChang rural Area
Chang Ki lee 3
0 graduate school of Medical science and engineering, Korea Advanced Institute of science and Technology (KAIsT) , Daejeon
1 PyeongChang health Center & County hospital , gangwon-Do
2 Department of Internal Medicine, Asan Medical Center, University of Ulsan College of Medicine , seoul
3 g oldman Urology Clinic , seoul, republic of Korea
4 g eriatric Center, s eoul n ational University Bundang hospital , gyeonggi-Do
PowerdbyTCPDF(ww.tcpdf.org) lee 1 *These authors contributed equally to this work Purpose: It is important to define lean muscle mass when diagnosing sarcopenia, but there is still controversy on the clinical implication of sarcopenia derived by height, weight, and body mass index (BMI) adjusted muscle mass indices. We aimed to evaluate the longitudinal clinical relevance of 3 sarcopenia definitions in the Korean population. Patients and methods: We conducted comprehensive geriatric assessments for 1,379 community-dwelling older participants in the Aging Study of PyeongChang Rural Area (ASPRA) cohort and followed them up prospectively for death, institutionalization, and disability every 3 months. Sarcopenia was defined using the Asian Working Group consensus algorithm, combining grip strength, gait speed, and muscle mass. Results: Among 1,343 participants (mean age: 76 years, 741 women) analyzed, there were 29 deaths and 89 institutionalizations during 22.0 ± 8.3 months follow-up (mean ± SD). All three muscle indices correlated to age and sex. All sarcopenia criteria with muscle mass indices of height, weight, and body mass index (BMI) adjustment significantly predicted death or institutionalization. However, when adjusted for age and sex, only the sarcopenia criteria with muscle mass index of height adjustment were significantly associated with major adverse health outcomes. Conclusion: Adjusting age and gender, the sarcopenia definition from the quintile-based muscle index of height adjustment could predict death or institutionalization in Korean community-
Il-Young Jang; 1; 2; * h ee-Won
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Sarcopenia is a common geriatric condition that is defined as a state of decreased
muscle mass and performance with aging. This condition has been recognized as an
independent clinical entity, of importance with regard to geriatric outcomes including
mortality and functional decline, leading to its inclusion in the International
Classification of Disease, Tenth Revision, Clinical Modification (ICD-10-CM) Code.1 In
addition, with global population aging, the pharmaceutical industry2,3 and
biomedical researchers4 are keen to elucidate treatable targets within the basic mechanisms
of sarcopenia. Therefore, establishing clinically relevant criteria for sarcopenia in a
specific population is more important than ever.
There have been numerous efforts to standardize the diagnostic algorithm of
sarcopenia, including the monumental European consensus guideline5 and the consensus
Clinical Interventions in Aging 2018:13 91–99 91
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report from the Asian working group.6 In Korea, after a report
that suggested Korean-specific cutoff values for weight- and
height-adjusted appendicular skeletal muscle mass (ASM)
from the Fourth Korean National Health and Nutritional
Examination Surveys (KNHANES),7 studies have assessed for
outcome relevance of various cutoff values and adjusting the
method of muscle mass.8,9 However, with the birth cohort effect
of the Korean population and the cultural background favoring
leanness among young women, ASM appears to have an
ageassociated increment in women.10 These controversies create a
need for a sarcopenia definition that reflects age and sex.
Furthermore, many studies that assessed clinical features
and outcome of sarcopenia in Korea choose muscle mass per
se as an independent variable, rather than muscle strength
or physical performance.11–13 Otherwise, they focused on a
metabolic profile or metabolic consequences such as fatty
liver diseases as outcomes, rather than geriatric outcomes
we hypothesized that we could find population-based cutoff
/w an points for each of the low-muscle-mass indices associated
tt:sph rsope with clinical outcomes. Therefore, we aimed to evaluate the
from roF clinical relevance of various definitions of sarcopenia from
de the geriatric perspective, in a prospective cohort of the Aging
lado Study of PyeongChang Rural Area (ASPRA) that is
represennow tative of general Korean rural-dwelling older people.
Patients and methods
study design and population
The ASPRA is a population-based, prospective cohort study
targeted to frailty and geriatric syndromes among
communitydwelling older adults in Korean rural areas. Detailed design
and methods pertaining to the ASPRA cohort are described
elsewhere.14 Briefly, the study area is in PyeongChang
County, Gangwon Province, South Korea, located 180 km
east of Seoul. Inclusion criteria were 1) age 65 years or older;
2) registered in the National Healthcare Service; 3)
ambulatory with or without an assistive device; 4) living at home;
and 5) able to provide informed consent. Exclusion criteria
were 1) living in a nursing home; 2) hospitalized; or 3)
bedridden and receiving nursing home-level care at home at the
time of enrollment. Between October 201
4 and August 2017
1,379 community-dwelling older adults participated in the
ASPRA cohort, which included over 90% of eligible older
adults living in the study area.14 All participants implemented
a comprehensive geriatric assessment every 12 months, and
health-related outcomes – including death,
institutionalization, and disability – were recorded every 3 months.
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A previous study showed that ASPRA participants have
very similar characteristics to the nationally representative
sample of South Korea – KNHANES (the Korea National
Health and Nutrition Examination Survey) – except for the
small difference in short educational period and higher
agricultural workforce ratio.14 These characteristics ensure the
appropriate generalizability of this population for descriptive
figures that can represent Korean rural-dwelling older people.
The Institutional Review Board of Asan Medical Center,
Seoul, Korea, approved the protocol for this study, and all
participants provided written informed consent.
To evaluate body composition including total mass and lean
mass, we used bioelectrical impedance analysis (InBody 620;
InBody, Seoul, Republic of Korea) with the use of
measuring frequencies of 5, 50, and 500 kHz. The device measured
the impedance of four limbs while participants were
standing and calculated the skeletal muscle mass. To minimize
interindividual differences, all participants were asked to fast
overnight. ASM was calculated as the sum of the lean mass of
both arms and legs provided from the manufacturer’s algorithm.
Previous studies have validated that bioelectrical impedance
analysis is comparable to dual-energy X-ray absorptiometry.15
To assess the handgrip strength (kg), we used a dynamometer
(T.K.K. 5401 Grip-D; Takei, Tokyo, Japan).16 Sitting
comfortably with arm bent 90° over the knee, participants were
asked to hold the dynamometer as strongly as possible.17
All tests were conducted two times at intervals of 1 minute
or more. The maximum value from the dominant arm was
used for the analysis.
To evaluate the usual gait speed, participants were instructed
to walk a total of 7 meters at a comfortable, usual, walking
speed in a flat indoor space. Trained nurses measured the
transit time of the 4-m distance from standing to the first
footstep at the 4-m line by using a standard digital stopwatch
and excluding an acceleration and deceleration interval of
1.5 m, respectively.6 Finally, the usual gait speed (m/s) was
calculated as the time taken to walk 4 m (m/s).18
Definition of sarcopenia
To compare known several sarcopenia definitions, low
muscle mass was defined as the sex-specific lowest quintile10
of ASM adjusted for height squared (ASM/ht2),6 weight
(ASM/wt),13 or BMI (ASM/BMI),19 respectively. We adopted
the definition of low muscle mass using quintiles because the
definition has been widely accepted by several sarcopenia
definitions.5 Additionally, low muscle strength was defined
as decreased handgrip strength of less than 26 kg for men and
of less than 18 kg for women.6 Low physical performance
was defined as slow gait of less than 0.8 m/s.6 By
combining muscle mass, strength, and physical performance, we
determined sarcopenic status by the consensus algorithm
from the Asian Working Group for Sarcopenia.6
To evaluate the functional status and common geriatric
conditions, a comprehensive geriatric assessment was
administered annually by trained nurses. To evaluate
disability, seven activities of daily living (ADL), including
bathing, continence, dressing, eating, toileting, transferring,
and washing face and hands, or 10 instrumental activities of
daily living (IADL), including food preparation, household
chores, going out a short distance, grooming, handling
finances, laundry, managing own medications, shopping,
transportation, and using a telephone, were interviewed.20
We assessed multimorbidity – defined as having 2 or more
of the 11 physician-diagnosed illnesses including angina,
arthritis, asthma, cancer, chronic lung disease, congestive
heart failure, diabetes, heart attack, hypertension, kidney
disease, and stroke. Depression was defined as a Korean
version of the Center for Epidemiological Studies Depression
(CES-D) scale greater than 20 points.21 Polypharmacy was
defined as taking 5 or more prescription medications.
In this study, major adverse health outcomes have been
defined as death or institutionalization. All participants were
traced to minor check up every 3 months as well as a major
follow-up every year. In interviews with participants or
family members, the outcome was recorded when they were
found to have died or had been institutionalized for longer
than 3 months.
Functional impairment was evaluated by ADL and IADL
assessment at baseline and follow-up. The occurrence of
disability was defined as the absence of disability in baseline
evaluation but disability in follow-up measurement.
Baseline participant characteristics were analyzed by the
independent t-test for continuous variables and the χ2 test for
categorical variables. Scatterplots and correlation analysis
using linear regression models were conducted to
evaluate the effect of age and sex on each muscle mass index.
We used unadjusted or age- and multimorbidity-adjusted
Cox proportional hazards models for men and women to
clarify the clinical relevance of each muscle index on
outcome, combining mortality and institutionalization due to
functional decline. In addition, we used logistic regression
analyses to evaluate whether sarcopenia criteria with each
muscle mass index can predict functional impairment of
ADL or IADL during follow-up periods. Statistical analyses
were conducted using STATA 15.0 (StataCorp, College
Station, TX, USA).
Baseline characteristics according to
3 sarcopenia definitions
Among data from 1,379 ASPRA’s participants, we excluded
36 people (14 men and 22 women) for missing data on
bioelectrical impedance analysis, grip strength, or gait speed.
Finally, 1,343 (602 men and 741 women) were analyzed
for this study. The mean age of participants analyzed was
76.0 years (standard deviation [SD] 6.5 years), and the mean
BMI was 24.6 (SD 3.4 kg/m2). During the mean follow-up
period of 22.0 months (SD 8.3 months), 29 participants died
and 89 participants were hospitalized over 3 months.
Baseline characteristics of the participants according
to the sarcopenia algorithms by 3 muscle mass indices are
shown in Table 1. Briefly, participants with sarcopenia
defined according to each muscle index were similar in age,
sex, and duration of formal education. With sarcopenia,
physical performance by SPPB score as well as frailty status
were worse. Furthermore, the status of common geriatric
syndromes including disability (both ADL and IADL),
depressive mood, cognitive dysfunction, and polypharmacy
was worse with the presence of sarcopenia.
Classification according to sex-specific
effects of appendicular skeletal muscle
To assess the contribution of age and sex effects, we
plotted the distribution of muscle mass indices calculated from
three sarcopenia definitions (Figure 1). When adjusting sex
in linear regression analysis, age was associated with each
muscle index: 1) ASM/ht2: standardized beta [β] =-0.267,
P,0.001; 2) ASM/wt: β=-0.157, P=0.001; and 3) ASM/
BMI: β=-0.201, P,0.001.
Thereafter, we classified muscle indices into four
categories by sex-specific quintiles. Quintile cutoff values of
muscle indices adjusted by height, weight, and BMI are
shown in Table 2.
Major health adverse events by each
To compare future major health adverse events by various
muscle indices, we first compared each of the Kaplan–
Meier curves of sarcopenia defined by the three muscle
indices (Figure 2). Regardless of the adjusting method of
muscle indices, the presence of sarcopenia was associated
with significantly higher mortality and institutionalization
We investigated the risk of major health adverse events
with the Cox proportional hazards model for men and
women (Table 3). In an unadjusted model in men, the hazard
ratios (HRs) for major health adverse events were 5.48
(95% confidence interval [CI] 3.22–9.36) with sarcopenia
criteria with muscle mass index of height adjustment, 3.32
(95% CI 1.89–5.84) with muscle mass index of weight
adjustment, and 3.84 (95% CI 2.22–6.66) with muscle mass index
of BMI adjustment. When adjusted for age and
multimorbidity, sarcopenia criteria with muscle mass index of height
adjustment still had the highest HR for major adverse health
outcome (HR 5.18, 95% CI 3.03–8.85). In an unadjusted
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Abbreviations: ADl, activities of daily living; AsM, appendicular skeletal muscle mass; BMI, body mass index; Chs, Cardiovascular health study; ht2, height square adjusted;
IADl, instrumental activity of daily living; K-FrAIl, the Korean version of the Fatigue, resistance, Ambulation, Illnesses, and loss of weight questionnaire; sD, standard
deviation; sPPB, short physical performance battery; wt, weight adjusted.
model in women, the HRs for major health adverse events
were 2.88 (95% CI 2.26–4.75) with sarcopenia criteria with
muscle mass index of height adjustment, 1.49 (95% CI
0.83–2.66) with muscle mass index of weight adjustment,
and 1.63 (95% CI 0.94–2.85) with muscle mass index of
BMI adjustment. When adjusted for age and multimorbidity,
only sarcopenia criteria with muscle mass index of height
adjustment was significantly associated with major adverse
health outcome (HR 2.16, 95% CI 1.28–3.65).
Occurrence of functional impairment
With regard to occurrences of functional impairment,
logistic regression analysis was conducted, with the outcome as
the newly developed ADL or IADL at the follow-up CGA.
Unadjusted odds ratios for the occurrence of ADL disability
were 1.65 (95% CI 1.07–2.54) from sarcopenia criteria with
height-adjusted muscle mass index, 1.68 (95% CI 1.08–2.61)
from the criteria with weight-adjusted muscle mass index, and
1.95 (95% CI 1.28–2.97) from the criteria with BMI-adjusted
muscle mass index, respectively. In a model adjusted for age
and sex, the odds ratios for ADL disability from sarcopenia
criteria with muscle mass indices of height, weight, and BMI
adjustment were 1.30 (95% CI 0.81–2.07), 1.42 (95% CI
0.90–2.26), and 1.65 (95% CI 1.05–2.59), respectively.
For the occurrence of IADL disability, the odds ratios were
2.97 (95% CI 1.84–4.78) from sarcopenia criteria with muscle
mass index of height adjustment, 3.28 (95% CI 2.02–5.33)
from the criteria with weight-adjusted muscle mass index, and
2.90 (95% CI 1.80–4.65) from the criteria with BMI-adjusted
muscle mass index, respectively. In an age- and sex-adjusted
model, the odds ratios for IADL disability from sarcopenia
criteria with muscle mass indices of height, weight, and BMI
adjustment were 2.15 (95% CI 1.30–3.57), 2.50 (95% CI
1.51–4.15), and 2.08 (95% CI 1.26–3.45), respectively.
In this study, we compared major health adverse outcomes
according to the three sarcopenia definitions in a 22-month
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follow-up of a rural community-dwelling cohort potentially
representative of general rural-dwelling older adults of
South Korea. We observed sex-specific distributions of
muscle indices adjusted by height, weight, and BMI. Moreover,
when combined with physical performances of gait speed
.rvdoepww ll.syeuon and grip strength, sarcopenia definitions using all three of
these adjustment methods for muscle indices had significant
hazard risks of major health adverse events in death or
institutionalization in men, even after age and
multimorbidity adjustment. For women, only sarcopenia defined using
muscle mass index of height adjustment was associated with
significantly increased risk for major health outcomes before
and after age and multimorbidity adjustment.
Ethnic differences in anthropometric parameters and
outcome relevance have caused researchers to establish
population-specific definitions of the decreased lean muscle
mass in many countries. Our cutoff points using the lower
quintile were ,6.439 kg/m2 for men and ,5.197 kg/m2 for
women in height-adjusted muscle mass index, and ,0.693 m2
for men and ,0.446 for women in the BMI-adjusted muscle
mass index, and comparable to reports from other countries.
Considering the height-adjusted muscle mass index,
bioelectrical analysis (BIA)-using cutoff points for decreased
muscle mass defined as 2SD lower than healthy young adults
were reported as ,8.87 kg/m2 for men and ,6.42 kg/m2 for
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women in Taiwan,22 ,7.0 kg/m2 for men and ,5.8 kg/m2 for
women in Japan,23 ,5.72 kg/m2 for men and ,4.82 kg/m2
forwomeninChina,24 and,6.75kg/m2 formenand,5.07kg/m2
for women in another report from Korea.25 In a study
that used the lowest quintile of the muscle mass index
for the definition of decreased muscle mass, cutoff points
were ,7.27 kg/m2 for men and ,5.46 kg/m2 for women in
Taiwan.26 With regard to the muscle index adjusted by BMI,
our cutoff points were 0.693 m2 for men and 0.466 m2 for
women, compared to 0.789 m2 for men and 0.512 m2 for
women from the original report of the FNIH sarcopenia
project.19 Cut-off points from the ASPRA population were
relatively lower than other studies, of which these
differences are probably due to the high participation rate of the
ASPRA cohort with lower selection bias from including
more frail participants from among community-dwelling
Varying definitions of sarcopenia have been proposed
by several authoritative research groups in order to diagnose
sarcopenia. In a long controversy, how to define the reduced
skeletal muscle mass was an important issue. In the past,
sarcopenia was defined as a state of decreased muscle mass, such
as a reduction of ASM of less than 2 SDs from the healthy
young adult population, or the lowest quintile value in the
study population.27–29 However, since muscle strength or
physical performance is more important in predicting health
outcome than ASM alone,30 the sarcopenia criteria – defined
as a combination of muscle mass with slowness and/or
weakness – proposed by the European working group and the
Asian group, has been widely applied.5,6 Recently, moreover,
the Sarcopenia Project of the National Institutes of Health
(FNIH) group has defined ASM/BMI as low lean mass
following analysis of nine large community-based cohorts.19
They primarily defined lean muscle mass in relation to body
composition and mobility limitation. However, various
definitions of sarcopenia, discussed above, have been reported in
different clinical implications, depending on the population,
age, socioeconomic status, or type of outcome.10,31–33 For
possible differences of muscle mass, strength, and physical
performance pertaining to specific populations, we should
adopt cutoff values and adjustment methods of muscle mass
indices and definitions of sarcopenia in a population-specific
There have been several reports of FNIH-defined
sarcopenia criteria predicting mortality or cognitive decline
in Koreans.36,37 Recently, FNIH-defined sarcopenia criteria
have been reported to predict death and adverse events from
I-Lan Longitudinal Aging Study in Taiwan.38 However, we
showed that only a sarcopenia definition with height-adjusted
muscle index was significantly associated with death or
institutionalization, rather than FNIH sarcopenia criteria
when adjusted for age and sex. This difference may be due
to heterogeneities in the characteristics of the study
population, outcome measures, and the duration of follow-up. In
contrast, with our secondary analysis for functional decline,
the FNIH definition consistently predicted the occurrence
of ADL or IADL disability even after adjusting for age
and sex. This similarity is probably due to the fact that the
FNIH definition is made with the mobility limitation as a
Our study has several strengths and limitations. First,
the ASPRA cohort is based on the Korean older population
living in rural communities. However, the demographic
characteristics of ASPRA share similarities with the national
representative sample – KNHANES – and has a high
participation rate of eligible older adults in the research area.14 All
measurement tools in ASPRA cohort are well standardized
and cover most geriatric syndromes. Second, for
measurement of muscle mass, this study used bioelectrical impedance
analysis which is known to be very accurate and reproducible
in evaluating skeletal muscle mass, and the standard method
for sarcopenia diagnosis by the authorized guideline.6,39
Third, the population-based ASPRA cohort does not include
laboratory or biomarker findings. Nevertheless, as in
previous cardiology studies of gait speed and clinical outcome,40,41
value of the study.
clinical indices have been reported to be as relevant as the
integrity of any part of the work is appropriately investigated
results of metabolic profiles composed of laboratory results.
and resolved. All authors have read and revised this
manuRather, this non-invasiveness also leads to a high retention
script. This manuscript is the final approved version from
rate per year of approximately 90% or more to increase the
all authors. All authors have reviewed and agreed to be
From this study, we provide distributions of muscle mass
indices that can be used in algorithms of sarcopenia, in a
nationwide representative rural-dwelling older population of
Korea for the first time. Moreover, we found that a sarcopenia
definition which combined grip strength and gait speed with
muscle mass index adjusted for height is most highly
associated with major adverse health outcome when adjusted for
age and multimorbidity in both men and women.
We are indebted to public health professionals and nurses
of PyeongChang County Hospital, Public Health Center,
and Community Health Posts for their administrative
support and help in enrollment, retention, and measurements.
We especially appreciate Hyelim Park, Seon-hee Cheon,
Chawoong Jeon, and Jae Kyoon Hwang from PyeongChang
The Aging Study of PyeongChang Rural Area was
supported by PyeongChang County Hospital, PyeongChang
County, Gangwon Province, Korea. The present study was
supported, in part, by Paul Park and Maeil Dairies Co., Ltd.
from the Asan Institute for Life Sciences and Corporate Relations
of the Asan Medical Center, Seoul, Republic of Korea.
Dr Hee-Won Jung was supported by a Global PhD
Fellowship Program through the National Research
Foundation of Korea funded by the Ministry of Education
Public health professionals and nurses of PyeongChang
County Hospital were involved in data collection, but they did
not have any role in the study design, analysis or
interpretation of data, in the writing of the report, or in the decision to
submit it for publication. Paul Park and Maeil Dairies Co.,
Ltd. did not have any role in the study design, in the
collection, analysis or interpretation of data, in the writing of the
report, or in the decision to submit it for publication.
All authors participated in designing the study concept,
undertook statistical analysis, data analysis, and
interpretation, and drafted the manuscript. They agree to be accountable
for all aspects of the work in ensuring that the accuracy or
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responsible for the process, accuracy, and integrity of all
parts of this manuscript.
The authors report no conflicts of interest in this work.
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