Korean J Fam Med. 2013;34:281-288 http://dx.doi.org/10.4082/kjfm.2013.34.4.

281

Original
Association between Sarcopenia, Bone Article
Density, and Health-Related Quality of Life
in Korean Men

Seon Won Go, Young Hwa Cha, Jung A Lee, Hye Soon Park*
Department of Family Medicine, Asan Medical Center, Ulsan University College of Medicine, Seoul, Korea

Background: Sarcopenia is the loss of muscle mass leading to decreased muscle strength, physical disability, and increased
mortality. The genesis of both sarcopenia and osteoporosis is multifactorial, and several factors that play a role in
osteoporosis are thought to contribute to sarcopenia. This study evaluated the association between sarcopenia and bone
density and health-related quality of life in Korean men.
Methods: We used the data of 1,397 men over 50 years of age from the 2009 Korean National Health and Nutrition
Examination Survey. Sarcopenia was defined as the appendicular skeletal muscle mass divided by height2 (kg/m2) < 2
standard deviations below the sex-specific mean for young adults. Health-related quality of life was measured by the
EuroQol-5 dimension (EQ-5D) instrument. Logistic regression analysis was performed to evaluate the relationship
between sarcopenia, bone density, and health-related quality of life.
Results: The T-score of the lumbar spine, total femur, and femur neck in bone mineral density in subjects with sarcopenia
were lower than those in subjects without sarcopenia. The score of the EQ-5D index was significantly lower and the rate
of having problems with individual components of health-related quality of life was higher in the sarcopenic group. After
adjustment for age and body mass index, the odds ratios (ORs) (95% confidence interval [CI]) for sarcopenia were 2.06
(1.07–3.96) in osteopenic subjects and 3.49 (1.52–8.02) in osteoporotic subjects, respectively. After adjustment, the total
score of the EQ-5D index was significantly lower in the sarcopenic subjects. The ORs (95% CI) for having problems of
mobility and usual activity of the EQ-5D descriptive system were 1.70 (1.02–2.84) and 1.90 (1.09–3.31), respectively.
Conclusion: Sarcopenia was associated with decreased bone mineral density in Korean men. In addition, sarcopenia was
related to poor quality of life, especially with regard to mobility and usual activity. Greater attention to and evaluation for
sarcopenia are needed in subjects showing low bone mineral density to prevent and manage poor quality of life.

Keywords: Sarcopenia; Osteoporosis; Metabolic Bone Diseases; Quality of Life

INTRODUCTION
Received: August 31, 2012, Accepted: June 18, 2013
*Corresponding Author: Hye Soon Park Sacopenia is the loss of muscle mass with age, which is known
Tel: +82-2-3010-3813, Fax: +82-2-3010-3815
to be related to decreased muscle strength, low physical activity,
E-mail: [email protected]
and increased mortality.1,2) In a previous study, sarcopenia increased
Korean Journal of Family Medicine the risk of having three or more disabilities on the instrumental
Copyright © 2013 The Korean Academy of Family Medicine
This is an open-access article distributed under the terms of
activities of daily living scale, one or more balance abnormalities,
the Creative Commons Attribution Non-Commercial License using a cane or walker, and falls.3) Several studies have reported
(http://creativecommons.org/licenses/by-nc/3.0) which permits that the prevalence of sarcopenia was 4% to 64%.4-7) The great
unrestricted noncommercial use, distribution, and reproduction in
range in prevalence is attributed to the fact that the definition of
any medium, provided the original work is properly cited.

Korean J Fam Med Vol. 34, No. 4 Jul 2013 | 281

Seon Won Go, et al: Sarcopenia, Bone Density, and Quality of Life

sarcopenia has not yet been firmly established, and the respective Disease Surveillance, Korea Centers for Disease Control and
techniques used for the measurement of lean mass and the Prevention, from 2007–2009. A total of 10,533 KNHANES IV
reference population were different. Aging is related to several sampled subjects were screened, for a response rate of 82.8%
anatomical changes including increased frailty, disability, and in 2009. All participants in this survey gave informed consent.
falls, as well as body composition changes, including decrease in This study analyzed data from 1,397 male subjects aged 50 years
8,9)
muscle and bone mass. Observational studies have reported or older among those who participated in the survey between
that muscle mass begins to decrease at approximately 1% per year January 2009 and December 2009, after excluding 83 incomplete
9,10)
following the fourth decade of life. respondents on the EuroQol-5 dimension (EQ-5D), 66 subjects
Low bone mineral density (BMD) and fracture risk are who did not have adequate blood samples, and 181 subjects who
10,11)
increasing with the aging of populations all over the world. did not conduct dual energy X-ray absorptiometry (DEXA)
In the US, 30% of men aged 50 years and older have femur measurements of BMD.
12)
neck osteopenia, and 2% have femur neck osteoporosis.
Osteoporosis in men is an underrecognized and undertreated 2. Lifestyle Questionnaire and Anthropometric
condition. Osteoporotic fractures in men are associated Measurements
with higher mortality and morbidity relative to women.13) Self-reported questionnaires were used to assess demographic
Undoubtedly, sarcopenia and osteoporosis will be a major characteristics and life style factors in participants. Dietary intake
problem in healthcare, imposing a great financial burden. including calcium was assessed using a 24-hour recall method.
The genesis of both sarcopenia and osteoporosis is Regular exercise was defined as exercise on a regular basis for
multifactorial. These causal factors include hormonal changes, more than 20 minutes at a time and more than three times per
low level of physical activity, low intake of dietary protein, and week. Smoking status was categorized as current smoker vs.
chronic inflammation.14-17) These common etiology may be nonsmoker. Alcohol consumption was classified according to
responsible for a positive relation between osteoporosis and the reported amount of drinks consumed on average per week.
sarcopenia, and it can be assumed that sarcopenia is a risk factor Alcohol drinking was defined as consumption of one or more
for osteoporosis, and that it is more prevalent among individuals drinks per drinking day at least one per month. Education level
having low BMD. was categorized as <6 years, 6–9 years, 9–12 years, and >12 years.
However, this hypothesis has not been proven universally. Household income was evaluated by equivalised gross household
One cross sectional study reported that sarcopenia and income per month, calculated by total household income per
18)
osteoporosis have no association. Although there were several month/√number of family members. Participants’ weight and
studies that evaluated the relationship between quality of life and height were measured according to standard procedures. Height
osteoporosis or frail fracture, studies of the relationship between was measured to the nearest 0.1 cm with the subject standing
sarcopenia and quality of life are few. Consequently, the purpose barefoot. Body weight was measured to the nearest 0.1 kg on a
of this study was to identify the association between sarcopenia balanced scale with the subject wearing a lightweight gown or
and BMD, as well as the relationship between sarcopenia and underwear. Body mass index (BMI) was calculated by dividing
quality of life in Korean men. body weight (kg) by height (m2). Waist circumference was
measured to the nearest 0.1 cm at the narrowest point between
the lowest rib and the uppermost lateral border of the right iliac
METHODS crest.

1. Study Subjects 3. Body Composition Analysis and Definition of

The Korea National Health and Nutrition Examination Sarcopenia, Osteopenia, and Osteoporosis
Survey (KNHANES) is a nationwide, cross-sectional health Total and regional BMD (g/cm2) and total and regional
survey. KNHANES IV was conducted by the Division of Chronic lean mass were measured by DEXA (DISCOVERY-W fan-

282 | Vol. 34, No. 4 Jul 2013 Korean J Fam Med

 Seon Won Go, et al: Sarcopenia, Bone Density, and Quality of Life

beam densitometer; Hologic, Bedford, MA, USA) using Table 1. Basic characteristics of study subjects (n = 1,397)

standard procedures. The stability of DEXA measurements was Without With

determined by a daily calibration with a phantom supplied from Characteristic sarcopenia sarcopenia P-value*
the manufacturer. The within-day coefficients of variation (%) for (n = 1,178) (n = 219)

duplicated measurements in 30 adults ranged from 0.84 to 2.29 Age (y) 60.4 ± 0.26 67.4 ± 0.87 <0.001
19) 2
among four examiners. Sarcopenia was defined as proposed BMI (kg/m ) 24.6 ± 0.09 19.9 ± 0.16 <0.001

by Baumgartner with appedicular lean mass (aLM) obtained as Waist circumference (cm) 86.8 ± 0.29 76.0 ± 0.56 <0.001
3)
the sum of lean mass in arms and legs, assuming that all nonfat Total body fat percentage (%) 22.2 ± 0.21 21.0 ± 0.60 0.007
and nonbone tissue was skeletal muscle divided by the squared Total body fat mass (kg) 15.3 ± 0.19 11.5 ± 0.39 <0.001
height (ht2); aLM/ht2. The cutoff point for our study subjects T-score of L-spine †
-0.57 ± 0.05 -1.53 ± 0.10 <0.001
was 6.93 kg/m2, equivalent to two standard deviations below a T-score of femur neck †
-0.60 ± 0.04 -1.66 ± 0.07 <0.001
young reference population. BMD was classified by the World T-score of total femur †
0.15 ± 0.03 -0.90 ± 0.07 <0.001
Health Organization criteria based on the T score of the lumbar Total energy (kcal/d) 2,168 ± 39 1,656 ± 50 <0.001
spine and/or femoral neck and/or total hip as follows: normal Carbohydrate (%) 66.8 ± 0.61 71.3 ± 0.97 <0.001
(T score > −1.0 SD), osteopenia (−1.0 ≥ T score > −2.5 SD), and
Fat (%) 14.5 ± 0.30 12.0 ± 0.54 <0.001
osteoporosis (T score ≤ −2.5 SD).
Protein (%) 13.9 ± 0.16 13.3 ± 0.33 0.056

Calcium intake (mg) 575.9 ± 15.3 420.6 ± 23.8 <0.001

4. Measurement of Health-Related Quality of ‡
Regular exercise 216 (39.2) 23 (41.0) 0.343
Life
Smoking 378 (34.9) 88 (43.1) 0.030
The EuroQol was used to evaluate health-related quality of
Alcohol drinking 787 (69.0) 116 (58.5) 0.005
life (HRQoL). The EQ-5D recorded the level of self-reported
Osteopenia 537 (43.8) 128 (56.9) <0.001
problems according to five dimensions (mobility, self-care, usual
Osteoporosis 63 (4.4) 67 (29.7) <0.001
activities, pain/discomfort, and anxiety/depression).20,21) Each
of the dimensions was assessed based on a single question with Education (y) <0.001

three response levels (no problems, some problems, and extreme >12 218 (22.2) 24 (12.4)

problems). In this paper, three levels of answers were classified 9–12 308 (28.3) 34 (17.1)

into two groups (problem absent/problem present). The 6–9 243 (20.6) 42 (21.2)

problem group included subjects who responded ‘some problem’ <6 402 (28.9) 118 (49.2)
and ‘extreme problem’ among three levels of severity. Using Household income §
<0.001
a combination of these items, a single health index score was Upper quartile 292 (30.2) 17 (11.1)
calculated using the Korea valuation set developed by the Korea 2nd 271 (24.3) 33 (15.3)
22)
Centers for Disease Control and Prevention. Scores of the EQ- 3rd 278 (21.7) 62 (33.3)
5D index range from −0.171 to 1, where 1 indicates no problems 4th 327 (23.8) 103 (40.2)
in any of the five dimensions, zero indicates death, and negative
Values are presented as mean ± SD or number (%).
values indicate a health status worse than death. *Calculated using t-test. †Age-adjusted means by analysis of
covariance. ‡Regular exercise was indicated when the subject
exercise on a regular basis for more than 20 minutes at a time and
5. Statistical Analysis
more than three times per week. §Household income was calculated
Statistical analyses were performed using SPSS ver. 18.0 by equivalised gross household income per month (the equivalised
(SPSS Inc., Chicago, IL, USA) which incorporates sample income = total household income per month/√number of family
weights and adjusts analyses for the complex sample design of the members) and grouped into four quartiles.

survey. The participants’ characteristics and EQ-5D index were

compared according to sarcopenia status using independent-

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Seon Won Go, et al: Sarcopenia, Bone Density, and Quality of Life

sample student’s t-tests for continuous measures and chi-square those without sarcopenia. They were more likely to smoke;
tests for categorical measures. The odds ratios (ORs) and 95% however, they were also less likely to drink alcohol. The T-score
confidence interval (CI) for sarcopenia according to BMD of L-spine, femur neck, and total femur were lower in subjects
(normal, osteopenia, and osteoporosis) and those for problems of with sarcopenia than those without sarcopenia. Prevalence
individual components of health-related quality of life according of osteopenia and osteoporosis was higher in subjects with
to sarcopenia were estimated using multivariate logistic regression sarcopenia than those without sarcopenia.
models adjusted for age, BMI, calcium intake, regular exercise,
smoking, alcohol, and education. Total EQ-5D index was 2. Score of EQ-5D Index and Individual
calculated using the analysis of covariance test after adjustment Components of EQ-5D Descriptive System in
for covariants. P < 0.05 was accepted as significant. Study Subjects
Table 2 showed the score of the EQ-5D index and individual
components of the EQ-5D descriptive system. The score of the
RESULTS EQ-5D index was significantly lower in subjects with sarcopenia
than those without sarcopenia. Subjects with sarcopenia showed
1. Basic Characteristics of the Study Subjects a significantly higher proportion of problems in all items of the
Basic characteristics of the study subjects are presented in EQ-5D descriptive system of HRQoL (mobility, self-care, usual
Table 1. Subjects with sarcopenia were older and had lower activity, pain & discomfort, anxiety & depression) than those
BMI, waist circumference, and total body fat mass. Total energy without sarcopenia.
and calcium intake in subjects with sarcopenia were lower than

Table 2. Score of EQ-5D index and individual components of EQ-5D descriptive system in study subjects

Variable Without sarcopenia (n = 1,178) With sarcopenia (n = 219) P-value

EQ-5D index (mean ± SE) 0.94 ± 0.003 0.88 ± 0.015 <0.001*

†
Problem of mobility (%) 16.4 33.0 <0.001‡

Problem† of self-care (%) 3.6 9.3 0.001‡

Problem† of usual activity (%) 9.0 25.9 <0.001‡

Problem† of pain/discomfort (%) 22.1 28.5 0.054‡

Problem† of anxiety/depression (%) 6.8 13.9 0.001‡

EQ-5D: EuroQol-5 dimension.

*Calculated using t-test. †Problem: ‘some or extreme’ among 3 level of the severity in EQ-5D descriptive system. ‡Calculated using chi-
square test.

Table 3. Prevalence and adjusted odds ratio (95% confidence interval) for sarcopenia according to bone mineral density

Prevalence of sarcopenia (%) Model 1* Model 2 Model 3

Normal 4.0 1 1 1

Osteopenia 17.4 2.06 (1.07–3.96) 1.54 (0.79–3.03) 1.53 (0.77–3.06)

Osteoporosis 52.3 3.49 (1.52–8.02) 2.30 (0.94–5.61) 2.14 (0.87–5.31)

Model 1 was adjusted for age and body mass index (BMI). Model 2 was adjusted for age, BMI, calcium intake, regular exercise, smoking,
and alcohol. Model 3 was adjusted for age, BMI, calcium intake, regular exercise, smoking, alcohol, and education.
*P for trend < 0.001 using multiple logistic regression analysis.

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 Seon Won Go, et al: Sarcopenia, Bone Density, and Quality of Life

3. Prevalence and Odds Ratios for Sarcopenia DISCUSSION

according to Bone Mineral Density
Table 3 shows the prevalence and ORs for sarcopenia This study demonstrated that the risk for sarcopenia increased
according to BMD. The prevalence of sarcopenia increased as as BMD decreased, and the subjects with sarcopenia were at
BMD decreased as follows: normal 4.0%, osteopenia 17.4%, and risk for decreased health-related quality of life. Several studies
osteoporosis 52.3%, respectively. After adjustment for age and have shown the relationship between BMD and sarcopenia. A
BMI, the ORs (95% CI) for having sarcopenia in the osteopenic previous study showed that lower BMD in pre/postmenopausal
and osteoporotic group were 2.06 (1.07–3.96) and 3.49 (1.52– women was related to a greater risk of sarcopenia, and the same
8.02), respectively (P for trend < 0.001). results were found after adjustment for diet, physical activity, and
hormone replacement therapy.23) According to a study of 313
4. Adjusted Score and Odds Ratios for Individual women with hip fracture, subjects with sarcopenia had a higher
Components of EQ-5D Descriptive System risk of osteoporosis.24) Their data showed significant association
according to Presence of Sarcopenia between sarcopenia and osteoporosis in a large sample of hip
Table 4 shows the adjusted score and ORs for individual fracture women. Other studies have demonstrated a positive
components of the EQ-5D descriptive system according to correlation among appendicular muscle mass and BMD, and
presence of sarcopenia. After adjustment, the total score of the decreased bending strength and lower cortical bones.25,26) Our
EQ-5D index was significantly lower in sarcopenic subjects. The data suggests that decreased BMD may be associated with
ORs (95% CI) for having problems of mobility and usual activity sarcopenia in men aged 50 or over. Sarcopenia is a marker of
of the EQ-5D descriptive system were 1.70 (1.02–2.84) and 1.90 falling, and bone loss indirectly influences the risk of fracture
(1.09–3.31), respectively, after adjusting for age, BMI, calcium because it causes impaired balance and falls.27) Therefore,
intake, regular exercise, smoking, alcohol, and education (P for combining low BMD and low muscle mass could indicate higher
trend < 0.001). fracture risk. The genesis of osteoporosis and sarcopenia is
multifactoral and complicated. Interestingly, several factors that
play a role in osteoporosis are thought to causing sarcopenia.

Table 4. Adjusted score and OR (95% CI) for individual components of EQ-5D descriptive system in subjects with sarcopenia compared to
subjects without sarcopenia

Model 1 P-value Model 2 P-value Model 3 P-value

Total score of EQ-5D

Without sarcopenia 0.94 (0.004) 0.001* 0.93 (0.004) 0.010* 0.93 (0.004) 0.037*

With sarcopenia 0.90 (0.011) 0.90 (0.012) 0.91 (0.011)

Individual components

Problem of mobility 1.93 (1.20–3.10) 0.007† 1.68 (1.01–2.80) 0.047† 1.70 (1.02–2.84) 0.043†

Problem of self care 1.60 (0.80–3.19) 0.184† 1.50 (0.74–3.04) 0.258† 1.51 (0.74–3.06) 0.256†

Problem of usual activity 2.13 (1.27–3.60) 0.005† 1.89 (1.08–3.29) 0.025† 1.90 (1.09–3.31) 0.024†

Problem of pain/discomfort 1.05 (0.68–1.61) 0.832† 0.84 (0.53–1.32) 0.447† 0.85 (0.54–1.34) 0.321†

Problem of anxiety/depression 1.15 (0.56–2.37) 0.141† 1.04 (0.49–2.21) 0.912† 1.07 (0.50–2.29) 0.870†

Values are presented as mean ± SE or OR (95% CI). Model 1 was adjusted for age and body mass index (BMI). Model 2 was adjusted for age,
BMI, calcium intake, regular exercise, smoking, and alcohol. Model 3 was adjusted for age, BMI, calcium intake, regular exercise, smoking,
alcohol, and education.
OR: odds ratio, CI: confidence interval, EQ-5D: EuroQol-5 dimension.
*Calculated using analysis of covariance test. †Calculated using multiple logistic regression analysis.

Korean J Fam Med Vol. 34, No. 4 Jul 2013 | 285

Seon Won Go, et al: Sarcopenia, Bone Density, and Quality of Life

These causal factors include low intake of dietary protein, low HRQoL (using by SF-36) and sarco-osteopenia that newly
physical activity, hormonal change, and chronic inflammation defined by BMD, muscle mass and grip length. Subjects with
14-17)
causing catabolic stimulation. In our study, we could not the limitation of activity related with sarcopenia showed lower
find any difference between subjects in consumption of dietary HRQoL.36) Several prospective studies have demonstrated that
protein and exercise. Because this study is a cross-sectional study, a high degree of physical activity has positive effects on muscle
there were limitations in interpreting the relationship between strength, and sarcopenia; and vice versa, a low level of physical
dietary intake or exercise status and sarcopenia. Smoking rate activity is related to decline in muscle strength and mass.37,38)
was higher in subjects with sarcopenia than those without Therefore, it seemed that sarcopenia affects mobility and usual
sarcopenia in our study. A recent study proposed that cigarette activity related to physical activity from among factors in HRQoL.
28)
smoking might induce skeletal muscle protein breakdown. In A previous study reported that sarcopenia is thought to
this study, subjects with sarcopenia showed a lower rate of alcohol impose an economic burden on healthcare services because it
consumption than those without sarcopenia. However, a decrease increases the risk of physical disability in elderly subjects.39) The
in lean body mass is commonly observed in alcohol abusers, and association between osteoporosis and sarcopenia suggests that
it is estimated that 40% to 60% of all adult abusers exhibit skeletal a further increase in healthcare expenses may be associated with
29)
muscle myopathy. The muscle wasting and myopathy associated sarcopenia, given relevant costs due to frailty fractures that are
with chronic alcohol abuse is due to an imbalance in protein suggested to be more common among subjects with sarcopenia.
30)
metabolism. Previous studies reported that sex hormones— Our study supports an economical approach to preventing
testosterone, estrogens, and dehydroepiandrosterone sulphate sarcopenia and decreased BMD in elderly people concurrently.
(DHEAS)—exert an important role in the age-related onset This study has some limitations. First, our study could not
31)
of sarcopenia. The decline in DHEAS may have a role in infer a cause-and effect relationship between sarcopenia and
the age-related dysregulation of testosterone in men in whom BMD and HRQoL. Also, it is difficult to know which sarcopenia
testosterone levels decrease by 1% per year, and bioavailable and low HRQoL precede or coincide. A prospective approach
testosterone decreases by 2% per year from age 30. Although this is needed when considering whether sarcopenia is a cause of
study could not demonstrate hormonal influence on sarcopenia, low HRQoL. Second, as we measured lifestyle factors using
a previous study showed that combined age-associated decline in questionnaires, we cannot exclude the possibility of inaccuracies.
sex hormone levels has a strong impact on mortality and osteo- Dietary intake, exercise, smoking, and alcohol consumption were
32)
metabolic diseases. During the aging process, loss of muscle measured from responses to a single question, and participants
strength and mass cause microarchitecture changes in bone and a may not have answered it precisely. Third, the DEXA scan
decrease in BMD. These common etiologies may account for the has some limitations in BMD evaluation in elderly men, like
positive association between sarcopenia and osteoporosis. spine osteoarthritis and aortic calcification that may cause
Our study showed that subjects with sarcopenia had lower underestimation of the real prevalence of low BMD. However,
HRQoL than those without sarcopenia. Moreover, subjects with this study might be the first study to evaluate the association
sarcopenia had significantly more problems with mobility and between sarcopenia and BMD and HRQoL using data from a
usual activity in the EQ-5D. Our study suggests that sarcopenia large representative sample of Korean men.
may have a greater influence on dimensions of physical In conclusion, our study demonstrated the risk for sarcopenia
functioning of HRQoL rather than social functioning or mental increased as BMD decreased in Korean men. In addition,
health. Loss of muscle mass and decrease in muscle strength sarcopenic subjects tend to suffer from poor quality of life,
through sarcopenia may induce discomfort during movement especially in mobility and usual activity. Attention and evaluation
and usual activity. Another study reported that sarcopenic obesity for sarcopenia are needed in subjects showing low BMD to
33)
was associated with decreased physical function, and thus it prevent and manage poor quality of life.
has been identified as an important cause of frailty among the
elderly.34,35) A recent study assessed the relationship between

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 Seon Won Go, et al: Sarcopenia, Bone Density, and Quality of Life

CONFLICT OF INTEREST Am J Obstet Gynecol 2006;194(2 Suppl):S3-11.

11. Brauer CA, Coca-Perraillon M, Cutler DM, Rosen AB.
No potential conflict of interest relevant to this article was Incidence and mortality of hip fractures in the United States.
reported. JAMA 2009;302:1573-9.
12. Looker AC, Melton LJ 3rd, Harris TB, Borrud LG, Shepherd
JA. Prevalence and trends in low femur bone density among
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