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Geriatr Gerontol Int 2014; 14 (Suppl. 1): 69–75

ORIGINAL ARTICLE

Prevalence and associated factors of sarcopenia and severe


sarcopenia in older Taiwanese living in rural community:
The Tianliao Old People study 04
Chih-Hsing Wu,1,9 Kuan-Ting Chen,2 Meng-Tzu Hou,3 Yin-Fan Chang,1 Chin-Sung Chang,1,8
Ping-Yen Liu,4,8 Shin-Jiuan Wu,5 Ching-Ju Chiu,9 I-Ming Jou6 and Chuan-Yu Chen7
1
Department of Family Medicine, 4Department of Internal Medicine, 6Department of Orthopedics, National Cheng Kung University
Hospital, 2Department of Medicine, College of Medicine, 8Graduate Institute of Clinical Medicine, College of Medicine, National Cheng
Kung University, 5Department of Food and Nutrition, Chung Hwa University of Medical Technology, Tainan, 9Institute of Gerontology,
National Cheng Kung University Medical College, Tainan, 3Department of Physical Therapy and Assistive Technology, National
Yang-Ming University, Taipei, and 7Department of Community Medicine, St. Martin De Poress Hospital, Chiayi, Taiwan

Aim: The aim of the present study was to show the prevalence and associated factors of sarcopenia and severe
sarcopenia in rural community-dwelling older Taiwanese.
Methods: Using the whole community sampling method, a total of 285 men and 264 women aged over 65 years
were randomly sampled (response rate = 50%) from Tianliao District, southern Taiwan, in 2012. Participants were
interviewed by trained investigators to complete a validated structural questionnaire. Body composition was measured
by bioelectrical impedance analysis, and skeletal muscle mass was estimated by Janssen’s equation. The Mini-
Nutritional Assessment (MNA) score, Short Portable Mental Status Questionnaire, grip strength, gait speed and short
physical performance battery (SPPB) were obtained by the standard procedures. Sarcopenia and severe sarcopenia
were defined according to the 2010 consensus of the Report of the European Working Group on Sarcopenia in Older
People.
Results: Of the 549 study participants, 39 (7.1%) were classified as having sarcopenia and 31 (5.6%) participants
were classified as having severe sarcopenia. Using multiple logistic regression models, the age, sex, working status,
waist circumference, body mass index, hypertensive history, MNA and SPPB score were independently associated
with different stages of sarcopenia.
Conclusions: Approximately one-fifth of community-dwelling older adults were facing the threat of sarcopenia in
southern Taiwan. The older age, female sex, lower body mass index, higher waist circumference, a history of
hypertension, lower MNA or SPPB score and not working regularly were associated factors for either sarcopenia or
severe sarcopenia. Geriatr Gerontol Int 2014; 14 (Suppl. 1): 69–75.

Keywords: bioelectrical impedance analysis, Mini-Nutritional Assessment, short physical performance battery,
skeletal muscle mass.

Introduction responsible for daily activities, sarcopenia has an influ-


ence on self-independence in activities of daily living,
Sarcopenia is named to reflect the status of decreased such as eating, taking a shower and walking,2–5 and
skeletal muscle mass (SMM) in aging people.1 As the results in adverse outcomes, including falls, hip frac-
SMM is one of the major human body components tures, comorbidities6–8 and mortality.9,10 Therefore, the
importance of sarcopenia is increasingly emphasized in
the aging society worldwide.6,11,12
Accepted for publication 2 December 2013. It is believed that sarcopenia is an economic burden
for both caregivers and the healthcare system in an
Correspondence: Dr Chih-Hsing Wu MD, Department of
Family Medicine, National Cheng Kung University Hospital, aging society.12 However, there are still limited studies
138 Sheng-Li Road, Tainan, 70428, Taiwan. Email: or inconsistent prevalence of sarcopenia in Chinese
paulo@mail.ncku.edu.tw populations.3,5,9,13–18 In contrast, most of the reports were

© 2014 Japan Geriatrics Society doi: 10.1111/ggi.12233 | 69


C-H Wu et al.

collected from subjects either living in nursing homes,15 264 women, aged 65–102 years, were enrolled (response
hospital-based3,18 or as volunteers.13,14 Few studies rate: 549/1098 = 50%) by the whole district sampling
focused on the systemic sampling of older adults living method.24 The sex distribution of the 549 respondents
in metropolitan areas.9,16,17 was not statistically different from the 1417 non-
Bioelectrical impedance analysis (BIA) is non- responders (P = 0.132). However, the mean age was
radiating, relatively cheap and portable, making it relatively younger for respondents (76.0 ± 6.2 vs 76.8 ±
possible to measure body composition in rural commu- 7.4 years, P = 0.001). For convenience and accessibility,
nities. Many studies have shown that BIA-derived skel- all the participants received the survey in five locally
etal muscle mass index (SMI) can be used to define designated examination centers evenly distributed in the
sarcopenia,3,13,19,20 it is plausible to use BIA rather than Tianliao District. This study was approved by the insti-
dual energy X-ray absorptiometry (DXA) to measure tute review board of National Cheng Kung University
the SMM in a community survey. Hospital (IRB number: B-ER-101-119). Each partici-
In 2010, the consensus of the Report of the European pant signed an informed consent before examination.
Working Group on Sarcopenia in Older People Participants were interviewed to complete a validated
(EWGSOP) redefined the criterion for sarcopenia in structural questionnaire,22,23 which included basic
which not only the muscle mass is taken into consider- characteristics, smoking and drinking habits, working
ation, but muscle strength and muscle performance status, and medical history. We defined participants to
are also considered for the definition of sarcopenia.21 have a smoking habit if they had smoked more than 100
Therefore, combined with muscle function and physical cigarettes and still smoked one pack (20 cigarettes) at
performance, the level of decreased SMM was newly least per month for more than 6 months, and alcohol
categorized as presarcopenia, sarcopenia and severe drinking was defined by if participants still drank one
sarcopenia.21 The aging population is endemic, espe- time per week for more than 6 months.23 A history of
cially in rural townships. However, the healthcare facili- hypertension or diabetes was assessed by referring to the
ties are relatively inadequate when compared with that self-reported physician’s diagnosis. Participants who
in metropolitan areas. Therefore, to obtain the status of still worked at a farm or had regular work were defined
sarcopenia in rural communities is urgent and impor- as working regularly. The long form Mini-Nutritional
tant for public health policy. To the best of our knowl- Assessment (MNA) was used as a screening tool to
edge, nearly none of the systemic sampling surveys of evaluate nutritional status.25,26 Cognitive function was
sarcopenia have focused on the rural communities in evaluated by the wrong answer of the 10-item Short
China or Taiwan. Furthermore, none of the studies Portable Mental Status Questionnaire (SPMSQ).27
have reported the different stages of sarcopenia and the
associated risk factors concomitantly. Anthropometry and body composition
The aims of the present study were to determine the
Bodyweight and standing height were measured by
prevalence of sarcopenia and severe sarcopenia of older
DETECTO (Detecto, Webb City, MO, USA), with par-
adults living in rural communities in southern Taiwan.
ticipants dressed in light clothing and barefoot. Body
The associated factors of different stages of sarcopenia
mass index (BMI) was calculated by bodyweight divided
were also evaluated accordingly. Through the compre-
by square of height (kg/m2). The waist circumference
hensive evaluation of sarcopenia in rural communities,
(WC) was measured (Gulick II; Gays Mills, WI, USA;
intervention and preventive strategy can be applied
to the nearest mm) midway between the lateral lower
appropriately.
rib margin and the superior anterior iliac crest at the
end of a gentle expiration phase.22 A single frequency
Methods
8-electrode bioelectrical impedance analysis (BIA)
device (BC-418; Tanita, Tokyo, Japan) was used to
In July 2012, a cross-sectional survey following the
measure body composition, which had been validated to
Tianliao Old People (TOP) study22,23 was carried out in
measure the SMM.28 SMM (kg) was estimated using the
Tianliao District, Kaohsiung City in southern Taiwan.
Janssen’s equation:20 SMM = ([Ht2 / R × 0.401] + [sex ×
In the 2012 census report, in the total population of
3.825) + (age × −0.071]) + 5.102, where height is in cm;
7800, 1966 subjects (25.2% of the total population)
resistance is in ohms; for sex, men = 1 and women = 0;
were aged 65 years and over. After excluding empty
and age is in years. SMM is divided by square of height
houses (n = 489), death (n = 40), non-ambulatory sub-
to obtain SMI (kg/m2) for defining low SMM and
jects (subjects with significant disabilities, such as
sarcopenia.2,3,21
handicapped cerebral vascular accident, cancerous
cachexia, unstable chronic diseases or psychiatric dis-
Physical performance
orders, severe arthritis or inflammatory disease, uncom-
fortable anorexia by any medications, n = 138) and Functional limitations were assessed by using the
non-reachable subjects (n = 201), a total of 285 men and short physical performance battery (SPPB).29 A higher

70 | © 2014 Japan Geriatrics Society


Sarcopenia in community-dwelling older Taiwanese

summary performance score represents a better perfor- ANOVA. Multiple logistic regression models were
mance, and vice versa.30 In the present study, the SPPB used to evaluate the independently associated factors
score was dichotomized as <9 or ≧9 for statistical analy- between different stages of sarcopenia. Statistical sig-
sis.29,30 Two tests (30 s separately) of grip strength nificance was defined as P < 0.05 for two-tailed analysis.
(Grip-D; TKK 5401, Tokyo, Japan) of the bilateral
hands were obtained for each participant. The maximal
Results
value of grip strength was used for the diagnosis of low
muscle function according to the corresponding cut-
All the basic characteristics are shown in Table 1. Of the
offs by BMI and sex.21 In short, the corresponding cut-
549 subjects, including 285 males and 264 females,
offs of low grip strength for men with BMI ≤24 kg/m2,
101 (18.4%) subjects with 35 (12.3%) men and 66
24.1∼28 kg/m2, and >28 kg/m2 were ≤29 kg, ≤ 30 kg,
(25.0%) women had SMI less than 7.70 and 5.67 kg/m2,
and ≤32 kg, respectively; for women with BMI ≤23 kg/
respectively.3 The prevalence of sarcopenia and severe
m2, 23.1∼26 kg/m2, 26.1∼29 kg/m2, and >29 kg/m2 were
sarcopenia were 7.1% (n = 39) and 5.6% (n = 31),
≤17 kg, ≤17.3 kg, ≤18 kg, and ≤21 kg, respectively.21
respectively. Women had a higher prevalence of sarco-
The gait speed was assessed by a 15-ft walking test. Low
penia and severe sarcopenia than men (Table 2). Non-
physical performance was determined when the gait
sarcopenic participants were younger, more likely to be
speed was ≤0.8 m/s.3
working regularly, had higher BMI, WC, SMI, MNA
and SPPB score, but lower gait speed and SPMSQ score
Definition of non-sarcopenia, sarcopenia and than sarcopenic and severe sarcopenic participants of
severe sarcopenia both sexes. No statistical difference of demographic
characteristics could be found between sarcopenia and
In the present study, we took the same young reference
severe sarcopenia.
values that have been validated by the National Health
Using multiple logistic regression models, the associ-
Research Institute in Taiwan.3 In short, 498 healthy
ated factors for different stages of sarcopenia are shown
males and 500 females aged 20–40 years were recruited
in Table 3. Age was a positive independent factor for all
for body composition assessment using the same BIA
stages of sarcopenia. BMI was a negative independent
(BC-418) with segmental measures for developing the
factor for all stages of sarcopenia. Sex was an indepen-
reference SMI.3 With the definition of low muscle mass
dent factor in models I, II and III. WC was shown to be
set at two standard deviations below the mean value of
an associated factor for all stages of sarcopenia, but was
SMI in the young reference groups, the cut-off points
only significant in model I. A lack of regular work was
for men and women were 7.70 and 5.67 kg/m2, respec-
an independent factor in model I. A History of hyper-
tively.3 Subjects were defined according to the 2010
tension and low MNA score were also the independent
consensus of Report of the European Working Group
factors in model III. Low SPPB score was also an inde-
on Sarcopenia in Older People.21 Those who had SMI
pendent factor in models II and IV. Other variables
higher than the cut-offs3 were classified as normal. Low
including WC, habitual smoking, drinking alcohol,
SMM (also named as presarcopenia) was defined as
history of diabetes and SPMSQ score showed no statis-
participants with SMI under two standard deviations of
tic significance in all different stages of sarcopenia.
the young reference of the same ancestry from 18 to 40
years-of-age.21 Sarcopenia was defined as participants
with low SMI and either low muscle function (reflected Discussion
by grip strength) or low physical performance (reflected
by walking speed). Severe sarcopenia was defined when Compared with studies carried out in Taiwan3,13,16,17 and
the aforementioned three conditions were present con- other countries,6,9,14,15,18,31,32 the prevalence of sarcopenia
comitantly.21 Normal and presarcopenia were reclassi- and severe sarcopenia in Tianliao, Kaohsiung, is con-
fied as non-sarcopenia for statistical analysis. sistently within the range of 5–30%. Interestingly, in the
present study, the prevalence of sarcopenia and severe
sarcopenia for women is notably higher than that of
Statistical analysis
men. Although men are supposed to have a higher
Statistical analysis was carried out by using the Statisti- prevalence of sarcopenia than women because of the
cal Package of Social Science for Windows software higher rate of muscular atrophy than women,11 the
Version 17 (SPSSWIN, version 17.0; Chicago, IL, prevalence might be inverted while using different diag-
USA). Continuous and categorical variables were nostic criteria of sarcopenia.16,33 As the present study
expressed as means ± SD and percentages, respectively. was carried out in a farming village, most of the male
The comparisons between groups in regard to categori- participants (50.2%) were still working more regularly
cal variables were analyzed using the χ2-test, and than the female participants (37.1%). Furthermore, gait
continuous variables were analyzed using one-way speed was higher in men than women (1.00 ± 0.28 m/s

© 2014 Japan Geriatrics Society | 71


72
|
Table 1 Demographic characteristics of 549 older Taiwanese adults living in a rural community

Total Normal Presarcopenia Non-sarcopenia Sarcopenia Severe P-value*


sarcopenia
n 549 448 31 479 39 31 –
Age (years) 76.0 ± 6.2 75.2 ± 5.9 76.4 ± 5.9 75.3 ± 5.9 80.4 ± 5.9† 81.8 ± 5.7‡ <0.001
Sex (male/female) 285/264 250/198 12/19 262/217 11/28† 12/19‡ 0.002
Height (cm) 154.6 ± 8.4 155.2 ± 8.2 156.1 ± 7.6 155.3 ± 8.2 150.8 ± 8.4† 149.4 ± 8.8‡ <0.001
Weight (kg) 58.8 ± 10.9 61.1 ± 10.2 52.7 ± 7.7 60.5 ± 10.3 48.7 ± 7.5† 45.5 ± 7.2‡ <0.001
Body mass index (kg/m2) 24.6 ± 4.1 25.4 ± 3.9 21.6 ± 2.3 25.1 ± 4.0 21.5 ± 3.0† 20.4 ± 2.4‡ <0.001
Waist circumference (cm) 87.0 ± 10.3 88.8 ± 9.9 80.8 ± 7.1 88.3 ± 9.9 78.9 ± 9.2† 78.3 ± 8.5‡ <0.001
Skeletal muscle mass (kg) 18.1 ± 4.9 19.0 ± 4.7 15.1 ± 3.9 18.8 ± 4.7 13.3 ± 3.1† 13.5 ± 3.8‡ <0.001
Skeletal muscle mass index (kg/m2) 7.4 ± 1.5 7.8 ± 1.4 6.1 ± 1.2 7.7 ± 1.4 5.8 ± 0.9† 5.9 ± 1.1‡ <0.001
Working regularly (%) 44.0 48.3 38.7 47.7 18.4† 19.4‡ <0.001
Habitual smoking (%) 26.2 28.3 19.4 27.7 10.5 22.6 0.062
C-H Wu et al.

Alcohol drinking (%) 16.5 17.9 12.9 17.6 13.2 3.2 0.095
History of hypertension (%) 49.5 51.3 22.6 49.5 55.3 41.9 0.546
History of diabetes (%) 17.2 17.9 16.1 17.8 13.2 12.9 0.618
Mini-Nutritional Assessment score 25.9 ± 2.6 26.2 ± 2.3 25.6 ± 2.7 26.2 ± 2.3 23.4 ± 3.4† 24.2 ± 2.6‡ <0.001
SPMSQ score 1.9 ± 1.9 1.6 ± 1.5 2.9 ± 2.2 1.7 ± 1.8 3.0 ± 2.5† 3.0 ± 2.4‡ <0.001
Gait speed (m/s) 0.92 ± 0.29 0.94 ± 0.29 1.10 ± 0.18 0.95 ± 0.28 0.82 ± 0.22† 0.59 ± 0.14‡ <0.001
SPPB score ≧9 (%) 72.2 76.4 93.5 77.5 56.8† 9.7‡ <0.001
*Comparison between non-sarcopenia, sarcopenia and severe sarcopenia. Continuous variables: one-way ANOVA. Categorical variables: χ2-test. Comparison between
non-sarcopenia and sarcopenia: †P < 0.001. Comparison between non-sarcopenia and severe sarcopenia: ‡P < 0.001. Comparison between sarcopenia and severe sarcopenia:
non-significance. Non-sarcopenia: combined with normal and presarcopenia. SPMSQ, short portable mental status questionnaire; SPPB, short physical performance
battery.

© 2014 Japan Geriatrics Society


Sarcopenia in community-dwelling older Taiwanese

Table 2 Prevalence of different stages of sarcopenia in 549 older


Taiwanese adults living in a rural community

Total Male Female P-value*


Case no. 549 285 264 –
Average age (years) 76.0 ± 6.2 76.2 ± 6.5 75.9 ± 5.8 0.633
Non-sarcopenia 479 (87.3%) 262 (91.9%) 217 (82.2%) <0.001
Normal 448 (81.7%) 250 (87.7%) 198 (75.0%) <0.001
Presarcopenia 31 (5.6%) 12 (4.2%) 19 (7.2%) 0.002
Sarcopenia 39 (7.1%) 11 (3.9%) 28 (10.6%) <0.001
Severe sarcopenia 31 (5.6%) 12 (4.2%) 19 (7.2%) 0.002
*Comparison between sex, χ2-test.

vs 0.83 ± 0.26 m/s), and grip strength was higher in men shown). However, participants who worked regularly
than women (33.0 ± 7.82 kg vs 20.4 ± 5.20 kg) in the or had a higher SPPB score showed a lower risk of
present study (data not shown). Therefore, women sarcopenia in the present study. Grip strength and gait
might have a higher prevalence of sarcopenia than speed are both the major surrogates of muscle function
men,16 but this paradox needs to be reconfirmed by and physical performance in combination with SMI for
further study. the diagnosis of sarcopenia.21 As the association between
Consistent with previous reports, age was the major grip strength, gait speed and sarcopenia was inconsistent
determinant of sarcopenia17,34 and physical perfor- in Chinese participants,5,35,41 the SPPB is not consistently
mance35 in the present study. Using the BIA-derived associated with different stages of sarcopenia. Neverthe-
SMM,3,13 the prevalence of sarcopenia defined by the less, physical performance should be measured univer-
EWGSOP definition21 was found to be substantially sally beyond measurements of SMM.35
increased with age in both men and women.3 A higher The present study had several limitations. First, the
BMI indicates better nutrition intake24 and relatively cross-sectional study did not allow us to identify any
higher SMM.11 Therefore, BMI is negatively correlated causal relationship. Second, only the ambulatory par-
with the prevalence of sarcopenia,6–8,15,16,18 which is con- ticipants were surveyed. Despite the 50% response rate
sistent with our findings. The fact that the MNA was and locally designated examination centers, the preva-
not independently associated with sarcopenia after it lence of presarcopenia (low SMM), sarcopenia and
was adjusted with BMI might reflect the superiority of severe sarcopenia might still be underestimated. Third,
BMI in relation to sarcopenia. Interestingly, the WC there are still some associated factors cannot be evalu-
showed a positive trend of low SMM after adjusting the ated adequately. As the Nagelkerke R2 values are 0.387–
BMI and major variables in multiple logistic model 0.563, most of the major factors were evaluated as
I. From the viewpoint of body composition, central possible in the present study. Finally, the comparison of
obesity might reflect the status of relatively higher bone the superiority of BIA-derived SMI with DXA-derived
mass and abdominal fat accumulation, but lower fat SMI in the evaluation of sarcopenia is still inconclusive.
free mass.22 Central obesity is a well-known risk factor However, as the awareness of sarcopenia in recent
of cardiovascular disease and metabolic aberrations. decade has improved, the cheap, portable and well-
Recently, SMI has been negatively correlated with validated BIA will become more popular in the near
insulin resistance or C-reactive protein, and might share future.
the pathophysiological mechanism with non-alcoholic In conclusion, the prevalence of sarcopenia and
fatty liver disease.36 Sarcopenia and WC could potenti- severe sarcopenia is 7.1% and 5.6%, respectively. Older
ate each other to induce hypertension.37 In summary, age, female sex, not working regularly, lower BMI,
the association between low SMM and lower BMI or higher WC, a history of hypertension, and lower MNA
higher WC is compatible with the concept of sarcopenic or SPPB score were independently associated with
obesity.33,38 The interrelationships between sarcopenia, sarcopenia and severe sarcopenia in older Taiwanese
sarcopenic obesity, hypertension and metabolic syn- adults living in a rural community.
drome have been emphasized,37,39 and warranted further
evaluation.
Studies have suggested that adequate physical activity Acknowledgment
might reduce the risk of sarcopenia.34,40 In the present
study, the median and mean weekly calorie expenditure This work was supported by the Ministry of Education,
(International Physical Activity Questionnaires) were Taiwan, R.O.C. under the NCKU Aim for the Top
4587.8 kcal and 7914.2 kcal, respectively (data not University Project (D101-35001). The authors thank

© 2014 Japan Geriatrics Society | 73


C-H Wu et al.

the staff of Tianliao district Public Health Center for

(0.319∼0.684)***
(1.054∼1.300)**

(0.561∼0.892)**
Model I: normal (n = 448) versus participants with low skeletal muscle mass (n = 101). Model II: non-sarcopenia (n = 479) versus sarcopenia and severe sarcopenia (n = 70).
their generous support, as well as Ms Yu-Chen Shih for
Odds ratio (95% CI)

Model III: non-sarcopenia (n = 479) versus sarcopenia (n = 39). Model IV: non-sarcopenia (n = 479) versus severe sarcopenia (n = 31). *P < 0.05, **P < 0.01, ***P < 0.001.
(0.929∼1.169)
(0.082∼1.485)

(0.201∼2.186)
(0.346∼8.746)
(0.018∼2.175)
(0.900∼1.407)
(0.328∼3.147)
(0.324∼1.413)
(0.839∼1.413)
her administrative assistance.

Disclosure statement
Model IV
(n = 510)
Table 3 Multiple logistic regression models of the risk factors for sarcopenia and severe sarcopenia in 549 older Taiwanese adults living in

0.563
1.170
1.042
0.348
0.467
0.662
1.740
0.195
1.125
1.016
1.284
1.089
0.707
The authors declare no conflict of interest.

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bioimpedance analysis system: improved phenotyping

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