Maturitas 133 (2020) 54–59

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Maturitas
journal homepage: www.elsevier.com/locate/maturitas

Low muscle mass is associated with osteoporosis: A nationwide population- T

based study
Sung-Young Janga, Jong Parkb, So-Yeon Ryub, Seong-Woo Choib,*
a
Department of Public Health, Graduate School of Chosun University, 309, Pilmun-daero, Dong-gu, Gwangju 61452, Republic of Korea
b
Department of Preventive Medicine, Chosun University Medical School, 309, Pilmun-daero, Dong-gu, Gwangju 61452, Republic of Korea

ARTICLE INFO ABSTRACT

Keywords: Objectives: To assess the association between low muscle mass and osteoporosis in the Korean general popula-
Low muscle mass tion.
Osteoporosis Methods: We analyzed 14,429 participants (6,261 men and 8,168 women) from the 2009–2011 Korean National
Lumbar spine Health and Nutrition Examination Survey (KNHANES) aged 20 years or more.
Femoral neck
Main outcome measure: The association of low muscle mass with osteoporosis was investigated using multi-
variate logistic regression models that included age, marital status, residence, current smoking, monthly
drinking, physical activities, strength exercise, comorbidity, and the use of dietary supplements, and in women
postmenopausal status and experience of pregnancy.
Results: After adjusting for covariates, low muscle mass was significantly associated with osteoporosis in the
lumbar spine and femoral neck in both men (lumbar spine: OR 1.73, 95 % CI 1.08–2.76; femoral neck: OR 3.39,
95 % CI 1.69–6.80) and women (lumbar spine: OR 1.52, 95 % CI 1.17–1.97; femoral neck: OR 2.09, 95 % CI
1.56–2.80). Also, the association between low muscle mass and osteoporosis was significant in men and women
in every age group except for men aged 50–64 years.
Conclusion: Low muscle mass was significantly associated with osteoporosis in both men and women for all age
groups, except for men aged 50–64 years.

1. Introduction
Osteoporosis is characterized by a decrease in bone density and
abnormal microstructure, which leads to reduced bone strength and
increases the risk of fractures [1]. With increasing age, the incidence of
osteoporosis and fractures increases [2]. While it is often considered a
disease of women, osteoporosis is also recognized as an important
health problem for men [3].
Muscle mass, a major component tissue loss in sarcopenia, decreases
with age, reducing exercise capacity and increasing the risk of falls and
fractures in older adults [4]. These changes also reduce the ability of
seniors to perform daily activities, leading to a loss of independence and
increasing the risk of death [5].
The most common physical changes with aging involve weakening
of the musculoskeletal system. Muscle and bone tissues are very closely
related anatomically; with age, these tissues weaken simultaneously,
causing low muscle mass and osteoporosis, with consequences such as
falls and fractures [6]. However, it is still unclear whether sarcopenia
including low muscle mass and osteoporosis should be regarded as one
disease or two [7]. Therefore, it is very important to clarify the re-
lationship between low muscle mass and osteoporosis for the preven-
tion and effective treatment of these diseases.
Studies evaluating the relationship between low muscle mass and
osteoporosis have not produced concordant results. Some studies found
a significant association between sarcopenia and osteoporosis [8,9], but
not others [10,11]. In yet another study, the associations differed ac-
cording to gender and menopausal status [12]. In addition, most studies
mainly evaluated the relationship between low muscle mass and os-
teoporosis in the elderly [11,13,14], and few have evaluated adults of
all ages. However, low muscle mass and osteoporosis are not a problem
for the elderly alone, especially in Korea, where vitamin D levels are
low in young people [15] and the risk of osteoporosis is increasing.
Research needs to examine the relationship between low muscle mass
and osteoporosis in adults of all ages.
Therefore, this study investigated the relationship between low
muscle mass and osteoporosis in Korean adults using the 2009–2011
Korea National Health and Nutrition Examination Survey (KNHANES).

⁎
Corresponding author.
E-mail address: jcsw74@hanmail.net (S.-W. Choi).

https://doi.org/10.1016/j.maturitas.2020.01.003
Received 16 October 2019; Received in revised form 9 December 2019; Accepted 7 January 2020
0378-5122/ © 2020 Elsevier B.V. All rights reserved.
S.-Y. Jang, et al.
2. Methods
2.1. Subjects
KNHANES is a nationwide cross-sectional survey conducted an-
nually by the Korea Centers for Disease Control and Prevention
(KCDCP). As previously published in detail [16], KNHANES uses a
rolling sampling design involving a complex, stratified, multistage,
probability-cluster survey of a representative sample of non-in-
stitutionalized Korean citizens residing in Korea. KNHANES consists of
three component surveys: the health interview, health examination,
and nutrition survey. The health interview and nutrition survey ques-
tionnaires are administered by trained interviewers, and the health
examinations are performed by trained medical staff. The KCDCP Ethics
Committee approved the study protocol (2009-01CON-03-2C, 2010-
02CON-21-C, 2011-02CON-06-C), and written informed consent was
obtained from all subjects or their parents.
There were 28,009 participants in the 2009–2011 KNHANES
(10,533 in 2009, 8,958 in 2010, and 8,518 in 2011), of whom 17,720
participated in both the health interview and health examination, in-
cluding whole-body dual-energy x-ray absorptiometry (DXA), and
15,585 were over 20 years of age. In total, 14,429 participants (6,261
men, 8,168 women) were analyzed, after excluding 1,156 subjects with
missing appendicular skeletal muscle mass (ASM) or hematological
data.
2.2. Data collection
Information on demographics and health behaviors was obtained
from the results of interviews by trained investigators. Anthropometric
information, such as height, weight, and body mass index (BMI), was
obtained from the survey results. Marital status was classified according
to the spouse’s current cohabitation status, and the residence area was
divided into ‘urban’ and ‘rural’. Current smoking was classified ac-
cording to the smoking status at the time of the investigation and
monthly drinking was classified according to last month’s drinking
status. Physical activity was defined as when the participant performed
strenuous exercise for more than 20 min at a time and more than three
times per week or moderate exercise for more than 30 min at a time and
more than five times per week or walking for more than 30 min at a
time and more than five times per week. Strength exercise was classi-
fied as ‘yes’ or ‘no’, depending on whether it was conducted more than
once a week. The comorbidities were classified by asking the subjects if
they had been diagnosed with hypertension, diabetes, dyslipidemia,
cardiovascular disease, cerebrovascular disease, arthritis, cancer, cir-
rhosis, or chronic renal failure.
The use of dietary supplements was classified according to whether
they had taken nutritional supplements for more than 2 weeks in the
past year. Experience of pregnancy was classified by the total number of
pregnancies to date, and postmenopausal was classified according to
menopause status.
2.3. Osteoporosis and low muscle mass
The bone mineral density (BMD) and body composition of the
participants were measured using DXA (Discovery-W fan-beam densit-
ometer; Hologic, MA, USA). Daily phantom scans were performed each
morning for quality control, and all BMD scans were conducted by well-
trained examiners using standardized procedures according to the
manufacturer’s recommended protocols. Examiners excluded scans
with insufficient scanning of metal implant, severe degenerative
change, or compression fracture. The BMD of the lumbar spine (L1-4)
and femoral neck were analyzed and osteoporosis was defined using the
World Health Organization (WHO) T-score criteria (T-score < –2.5).
ASM was calculated as the sum of the muscle mass in the arms and
legs and the sarcopenia index (SI) was calculated as ASM (kg)/BMI (kg/
55
Maturitas 133 (2020) 54–59
m²). Low muscle mass was defined as SI < 0.789 in men and < 0.521 in
women based on the criteria of the Foundation of the National Institute
of Health (FNIH) Sarcopenia Project [17].
2.4. Statistical analysis
The data were analyzed using SPSS (ver. 23.0; IBM, Armonk, NY,
USA). The responses were weighted by reference to the multistage,
complex, probability sampling design. Data are expressed as absolute
numbers and estimated percentages (with standard errors [SEs]) or as
means ± standard deviation (SD). The χ2 test or Student’s t-test was
used to evaluate the differences in demographic and clinical char-
acteristics according to gender and osteoporosis. Multivariate logistic
regression analysis was used to investigate the association of low
muscle mass with osteoporosis. Model 1 was adjusted for age, marital
status, and residence. Model 2 was also adjusted for current smoking,
monthly drinking, physical activities, strength exercise, comorbidity,
and the use of dietary supplements and postmenopausal status and
experience of pregnancy in women. A value of P < 0.05 was considered
indicative of statistical significance.
3. Results
Table 1 shows the general characteristics of the subjects. The pre-
valence of osteoporosis and low muscle mass was 8.9 % and 9.9 %,
respectively. Among the subjects, 27.0 % currently smoked, 59.3 % had
consumed alcohol in the past month, and 53.1 % were physically active.
The male subjects were younger, were more often married, smoked and
drank more, were more physically active, performed more strength
exercises, had fewer comorbidities, used fewer dietary supplements,
and fewer had osteoporosis and low muscle mass than the female
subjects (P < 0.001). The mean height, weight, and waist cir-
cumference were higher in men than in women (P < 0.001).
Table 2 summarizes the subjects’ characteristics according to os-
teoporosis. In both men and women, the subjects with osteoporosis
were older, less often urban residents, drank less, performed fewer
strength exercises, had more comorbidities, used fewer dietary sup-
plements, and more often had low muscle mass than the subjects
without osteoporosis. In men, the subjects with osteoporosis were
married more often than the subjects without osteoporosis. In women,
the subjects with osteoporosis were married less often, less physically
active, more often postmenopausal, and had had more pregnancies than
the subjects without osteoporosis. The mean height and weight were
higher in the subjects with osteoporosis in both men and women; the
mean waist circumference was smaller in men with osteoporosis, but
higher in women with osteoporosis.
Table 3 shows the associations between low muscle mass and os-
teoporosis. In men, the crude odds ratios (ORs) indicated that the as-
sociation between low muscle mass and osteoporosis was significant in
both the lumbar region (OR 2.17, 95 % confidence interval [CI]
1.50–3.14) and femoral neck (OR 6.44, 95 % CI 3.98–10.43). After
adjusting for age, survey year, marital status, residence, waist cir-
cumference, current smoking, month drinking, physical activity,
strength exercise, comorbidity, and the use of dietary supplements
(Model 3), the significant association between osteoporosis and low
muscle mass remained in both the lumbar area (OR 1.73, 95 % CI
1.08–2.76) and femoral neck (OR 3.39, 95 % CI 1.69–6.80). In women,
the association between low muscle mass and osteoporosis was sig-
nificant in both the lumbar area (OR 3.57, 95 % CI 2.90–4.39) and
femoral neck (OR 4.72, 95 % CI 3.76–5.92). After adjusting for the
same covariates and postmenopausal status and experience of preg-
nancy (Model 3), the significant association between osteoporosis and
low muscle mass remained in both the lumbar area (OR 1.52, 95 % CI
1.17–1.97) and femoral neck (OR 2.09, 95 % CI 1.56–2.80).
Table 4 shows the associations between low muscle mass and os-
teoporosis stratified by age group. In men, after adjusting for the same
S.-Y. Jang, et al. Maturitas 133 (2020) 54–59

Table 1 Baumgartner et al. diagnosed low muscle mass as present when the
General characteristics of subjects. ASM divided by the square of the height [ASM (kg)/Height² (m²)] was
Variables Total Male Female p-value below two standard deviations of the mean of the young control group
(n = (n = (n = [18]. Other investigators divided ASM by BMI [ASM (kg)/BMI (kg/m2)]
14,429) 6,261) 8,168) and diagnosed low muscle mass as present if it was below two standard
deviations of the mean of the young control group [19]. The FNIH
Age (years) 45.3 ± 0.3 44.1 ± 46.4 ± 0.3 < 0.001
0.3
Sarcopenia Project integrated data for nine cohorts and gave the criteria
Survey year 0.513 for diagnosing low muscle mass as ASM/BMI < 0.789 in men and <
2009 47.9 (1.1) 47.5 (1.2) 48.4 (1.1) 0.521 in women without comparison with a young reference group
2010 45.1 (1.7) 45.5 (1.8) 44.7 (1.7) [17]. In Korea, research on low muscle mass using data from the
2011 6.9 (0.8) 7.0 (0.9) 6.9 (0.8)
KNHANES has given various results depending on the diagnostic cri-
Married (%) 69.6 (0.7) 71.5 (0.9) 67.7 (0.8) < 0.001
Urban dwellers (%) 79.8 (1.9) 79.8 (2.0) 79.9 (1.9) 0.845 teria. Using the 2008–2011 KNHANES data, the prevalence of low
Height(cm) 163.9 ± 0.1 170.8 ± 157.1 ± < 0.001 muscle mass defined by ASM/Weight in adults over 20 years of age was
0.1 0.1 26.8 % [20], which was significantly higher than our result. In a study
Weight(kg) 63.8 ± 0.1 70.3 ± 57.4 ± 0.1 < 0.001
using the 2008–2009 KNHANES data, the prevalence of low muscle
0.2
Waist circumference (cm) 81.0 ± 0.1 84.1 ± 77.8 ± 0.2 < 0.001
mass in adults over 20 years was 12.4 % for men and 0.1 % for women
0.2 defined by ASM/Weight, but 9.7 % for men and 11.8 % for women
Current smoking (%) 27.0 (0.5) 47.4 (0.8) 6.5 (0.4) < 0.001 defined by ASM/Height² [21], which was similar to our result. Re-
Monthly Drinking (%) 59.3 (0.6) 77.2 (0.7) 41.3 (0.7) < 0.001 cently, the Asian Working Group for Sarcopenia (AWGS) defined the
Physical activitya (%) 53.1 (0.6) 55.7 (0.8) 50.5 (0.7) < 0.001
criteria for low muscle mass using DXA as ASM/Height² < 7.0 kg/m2
Strength exercise (%) 28.7 (0.6) 40.2 (0.9) 17.1 (0.5) < 0.001
Comorbidityb (%) 29.1 (0.6) 25.8 (0.7) 32.4 (0.7) < 0.001 for men and < 5.4 kg/m2 for women [22]. According to the 2008–2011
Use of dietary supplementsc 32.3 (0.6) 25.9 (0.8) 38.0 (0.8) < 0.001 KNHANES data analysis using the AWGS definition of low muscle mass,
(%) the prevalence of low muscle mass was 22.1 % in women over 65 years
Postmenopausal (%) – 37.4 (0.8) of age [23]. In our study, the prevalence of low muscle mass in women
Experience of pregnancyd – 78.8 (0.7)
(%)
over 65 years was 31.7 % using the AWGS criterion and 23.7 % using
Osteoporosis (%) 8.9 (0.3) 3.5 (0.3) 14.3 (0.5) < 0.001 the FNIH criterion.
Low muscle mass (%) 9.9 (0.4) 8.7 (0.5) 11.2 (0.6) < 0.001 We found significant associations between low muscle mass and
osteoporosis in both men and women. Previous studies have some
All values are presented as estimated percentage (standard error) or mean ± discordance regarding the association between sarcopenia and osteo-
standard deviation.
a porosis. In a study of 590 Finnish postmenopausal women [8] the au-
Physically active was indicated as ‘yes’ when the participant performed
thors defined sarcopenia using three components (low muscle mass,
moderate or strenuous exercise or walk on a regular basis (for more than 20 min
at a time and more than three times per week in the case of strenuous exercise; grip strength, and walking time) and reported that low muscle mass was
for more than 30 min at a time and more than five times per week in the case of significantly associated with osteoporosis. In a study of 2,479 elderly
moderate exercise; for more than 30 min at a time and more than five times per Koreans, after adjusting for the covariates, low muscle mass was sig-
week in the case of walk). nificantly associated with osteoporosis in men, but not in women [13].
b
Comorbidity were included hypertension, diabetes mellitus, dyslipidemia, In another study using 213 healthy American women aged between 17
cardiovascular disease, cerebral vascular disease, arthritis, cancer, liver cir- and 77, low muscle mass was not significantly related with BMD [10].
rhosis and renal insufficiency. Although, it is difficult to explain these discrepancies, there are some
c
Use of dietary supplements was defined as taking them regularly, ie, for plausible explanations. First, differences in the subjects’ demographics,
longer than 2 weeks during the previous 1 year.
d
such as sex, age, ethnicity, and menopausal status, might contribute to
Experience of pregnancy was defined when the a subject had ever been
the discordance. Second, as mentioned above, the definition of low
pregnant including normal pregnancy, ectopic pregnancy, still birth, sponta-
muscle mass varies across studies.
neous abortion, and induced abortion.
Low muscle mass and osteoporosis have been recognized as health
problems in elderly people because both increase with age. Therefore,
covariates (Model 3), the association between osteoporosis and low
most previous studies have examined the elderly [8,11,13,14]. How-
muscle mass was significant in subjects aged < 50 years (OR 7.74, 95 %
ever, since muscle volume decreases after the age of 30 years [24], it
CI 2.63–22.79) and ≥ 65 years (OR 1.80, 95 % CI 1.10–2.93), but not
cannot simply be regarded as a problem of the elderly. In Thailand, the
for those 50–64 years. In women, after adjusting for the same covariates
prevalence of low muscle mass was 15 % and 25 % in those in their 20 s
plus postmenopausal status and experience of pregnancy (Model 3), the
and 30 s, respectively [25], while the prevalence of low muscle mass in
association between osteoporosis and low muscle mass was significant
Korea was 19.2 % in those in their 20–30 s [20]. When stratified by age
in all age groups (< 50 years: OR 3.97, 95 % CI 1.39–11.32; 50–64
group, we found a robust significant association between low muscle
years: OR 1.67, 95 % CI 1.12–2.48; ≥ 65 years: OR 1.42, 95 % CI
mass and osteoporosis in all age groups. Only a few studies have in-
1.04–1.95).
vestigated the relationship between low muscle mass and osteoporosis
at all ages, including young adults. In another study of a general po-
4. Discussion pulation of 17,891 individuals older than 18 years, low muscle mass
was significantly associated with osteoporosis [12]. However, those
This study used the 2009–2011 KNHANES data to study the asso- authors did not report the association between low muscle mass and
ciations between osteoporosis and low muscle mass in the Korean osteoporosis by age group, because they did not perform stratification
general population aged 20 years and over. After adjusting for the analysis according to age groups.
covariates, low muscle mass was significantly associated with osteo- There are several possible explanations for the mechanism under-
porosis in both men and women. The significant association between lying the association between low muscle mass and osteoporosis. First,
osteoporosis and low muscle mass remained in all age groups, except muscle contraction provides direct mechanical stimulation to bone,
for men 50–64 years. promoting osteogenesis [26]. Second, low muscle mass and osteo-
We found that the prevalence of low muscle mass in Korean adults porosis share common pathophysiological pathways, genetic poly-
aged 20 and older was 8.7 % for men and 11.2 % for women. There is morphisms, endocrine disorders, malnutrition, and obesity [27]. Third,
no consensus criterion for the clinical diagnosis of low muscle mass. low muscle mass and osteoporosis are linked by inflammatory

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Table 2
Characteristics of subjects stratified by gender according to osteoporosis.
Variables Male p-value Female p-value

Non-osteoporosis Osteoporosis Non-osteoporosis Osteoporosis

(n = 5,945) (n = 316) (n = 6,656) (n = 1,512)

Age (years) 43.5 ± 0.3 60.8 ± 1.2 < 0.001 42.9 ± 0.3 67.3 ± 0.5 < 0.001
Survey year 0.332 0.962
2009 47.5 (1.3) 47.5 (3.7) 48.3 (1.2) 48.5 (2.0)
2010 45.6 (1.8) 43.1 (4.1) 44.8 (1.7) 44.5 (2.5)
2011 6.9 (0.9) 9.5 (2.1) 6.9 (0.9) 7.1 (1.1)
Married (%) 71.0 (1.0) 84.5 (2.5) < 0.001 70.2 (0.9) 52.4 (1.6) < 0.001
Urban dwellers (%) 80.1 (2.0) 70.2 (3.9) 0.001 81.9 (1.9) 67.7 (2.9) < 0.001
Height(cm) 171.0 ± 0.1 164.7 ± 0.5 < 0.001 158.2 ± 0.1 150.8 ± 0.2 < 0.001
Weight(kg) 70.7 ± 0.2 58.1 ± 0.8 < 0.001 58.1 ± 0.1 52.9 ± 0.3 < 0.001
Waist circumference (cm) 84.3 ± 0.2 78.7 ± 0.7 < 0.001 77.5 ± 0.2 80.2 ± 0.3 < 0.001
Current smoking (%) 47.6 (0.8) 42.6 (3.4) 0.152 6.7 (0.4) 5.1 (0.7) 0.059
Monthly Drinking (%) 77.8 (0.7) 62.1 (3.3) < 0.001 45.0 (0.8) 19.0 (1.4) < 0.001
Physical activitya (%) 55.8 (0.8) 53.2 (3.5) 0.462 51.3 (0.8) 45.3 (1.7) 0.001
Strength exercise (%) 40.7 (0.9) 25.2 (3.4) < 0.001 18.7 (0.6) 7.5 (0.9) < 0.001
Comorbidityb (%) 25.3 (0.7) 41.5 (3.6) < 0.001 27.0 (0.7) 64.5 (1.5) < 0.001
Use of dietary supplementsc (%) 26.1 (0.8) 19.2 (2.5) 0.015 38.9 (0.8) 32.6 (1.7) 0.001
Postmenopausal (%) – – – 28.8 (0.8) 88.5 (1.1) < 0.001
Experience of pregnancyd (%) – – – 76.6 (0.8) 91.8 (1.0) < 0.001
Low muscle mass (%) 8.3 (0.5) 19.9 (2.5) < 0.001 8.4 (0.5) 27.9 (1.7) < 0.001

All values are presented as estimated percentage (standard error) or mean ± standard deviation.
a
Physically active was indicated as ‘yes’ when the participant performed moderate or strenuous exercise or walk on a regular basis (for more than 20 min at a time
and more than three times per week in the case of strenuous exercise; for more than 30 min at a time and more than five times per week in the case of moderate
exercise; for more than 30 min at a time and more than five times per week in the case of walk).
b
Comorbidity were included hypertension, diabetes mellitus, dyslipidemia, cardiovascular disease, cerebral vascular disease, arthritis, cancer, liver cirrhosis and
renal insufficiency.
c
Use of dietary supplements was defined as taking them regularly, ie, for longer than 2 weeks during the previous 1 year.
d
Experience of pregnancy was defined when the a subject had ever been pregnant including normal pregnancy, ectopic pregnancy, still birth, spontaneous
abortion, and induced abortion.

cytokines, such as interleukin-6 and tumor necrosis factor alpha [28].
Fourth, bone and muscle interact biochemically via paracrine and en-
docrine communication as “bone–muscle talk”, involving osteocalcin
[29], vascular endothelial growth factor [30], insulin-like growth
factor-1, osteoglycin, fibroblast growth factor-2, myostatin [31].
Muscle and bone tissues are interconnected with each other not only
anatomically, but also metabolically and chemically [32]. Recently
some researchers demonstrated the close link between osteoporosis and
sarcopenia (low muscle mass and low muscle function) and suggested
the concept of osteosarcopenia to describe patients suffering from both
osteoporosis and sarcopenia [33]. In previous study, the patients of
osteosarcopenia were at a higher risk for fractures compared to them of
osteoporosis and sarcopenia [14]. Clinically, the activities to reduce fall
and fracture risk, such as nutritional evaluation, vitamin D assessment,
muscle strength and balance training, etc. should be recommended for
osteosarcopenia patients [33]. In addition, DXA scans is recommended
every two years for low-risk patients and once a year for high-risk
patients [34].
We found that low muscle mass was more strongly associated with
osteoporosis in the femoral neck than in the lumbar region. The lumbar
spine consists of spongy bone, while the femoral neck is cortical bone;
this is thought to have influenced the difference in the association.
Vitamin D has a greater effect on cortical bone than spongy bone [35]
and studies have shown that vitamin D has a stronger association with
BMD in the femur neck than that in the lumbar spine [36].
There are some limitations to this study. First, it is difficult to de-
monstrate causal relationships because it is a cross-sectional study.
Second, new guidelines from the 2018 EWGSOP proposed measuring
muscle strength or muscle performance, as well as muscle mass, when
diagnosing sarcopenia [37]. However, KNHANES did not measure
muscle strength or muscle performance. Third, KNHANES excludes
patients admitted to nursing homes or hospitals, so the number of pa-
tients with low muscle mass or osteoporosis may have been under-
estimated. However, this study is meaningful in that it shows the

Table 3
The associations between sarcopenia and osteoporosis.
Variables Model 1a Model 2b Model 3c
OR(95%CI) OR(95%CI) OR (95%CI)

Men Lumbar Low muscle mass 2.17 (1.50–3.14) 0.84 (0.55–1.28) 1.73 (1.08–2.76)
Normal reference reference reference
Femoral neck Low muscle mass 6.44 (3.98–10.43) 1.30 (0.74–2.29) 3.39 (1.69–6.80)
Normal reference reference reference
Women Lumbar Low muscle mass 3.57 (2.90–4.39) 0.98 (0.76–1.25) 1.52 (1.17–1.97)
Normal reference reference reference
Femoral neck Low muscle mass 4.72 (3.76–5.92) 1.24 (0.97–1.58) 2.09 (1.56–2.80)
Normal reference reference reference

a
Non-adjusted.
b
Adjusted by age, survey year, marital status and residence.
c
Adjusted by Model 2 variables plus waist circumference, current smoking, month drinking, physical activity, strength exercise, comorbidity, use of dietary
supplements, and additionally postmenopausal, experience of pregnancy in women.

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S.-Y. Jang, et al. Maturitas 133 (2020) 54–59

Table 4
The associations between sarcopenia and osteoporosis stratified by age groups.
Variables Model 1a Model 2b Model 3c
OR(95 %CI) OR(95 %CI) OR (95 %CI)

Men < 50 years Low muscle mass 3.29 (1.16–9.29) 3.15 (1.10–8.98) 7.74 (2.63–22.79)
Normal reference reference reference
50–64 years Low muscle mass 0.69 (0.29–1.61) 0.63 (0.26–1.55) 1.07 (0.45–2.58)
Normal reference reference reference
≥65 years Low muscle mass 1.18 (0.79–1.76) 1.22 (0.81–1.85) 1.80 (1.10–2.93)
Normal reference reference reference
Women < 50 years Low muscle mass 2.65 (1.02–6.93) 2.55 (0.98–6.62) 3.97 (1.39–11.32)
Normal reference reference reference
50–64 years Low muscle mass 1.51 (1.06–2.16) 1.50 (1.05–2.15) 1.67 (1.12–2.48)
Normal reference reference reference
≥65 years Low muscle mass 1.19 (0.91–1.57) 1.14 (0.86–1.50) 1.42 (1.04–1.95)
Normal reference reference reference

a
Non-adjusted.
b
Adjusted by survey year, marital status and residence.
c
Adjusted by Model 2 variables plus waist circumference, current smoking, month drinking, physical activity, strength exercise, comorbidity, use of dietary
supplements, and additionally postmenopausal, experience of pregnancy in women.

relationship between low muscle mass and osteoporosis in adults using
representative data from Korea.
In conclusion, after adjusting for the covariates, low muscle mass
was significantly associated with osteoporosis in both men and women
and these significant associations between osteoporosis and low muscle
mass remained in all age groups, except for men 50–64 years.
Contributors
Sung-Young Jang designed the study, performed the assessment,
analyzed and interpreted the data and drafted the manuscript.
Jong Park interpreted the data, performed the assessment, analyzed
and interpreted the data, and reviewed the manuscript.
So-Yeon Ryu performed the assessment and reviewed the manu-
script.
Seong-Woo Choi designed and supervised the study, interpreted the
data, and edited the manuscript.
Conflict of interest
The authors declare that they have no conflict of interest.
Funding
No external funding was received for this study.
Ethics
The KCDCP Ethics Committee approved the study protocol (2009-
01CON-03-2C, 2010-02CON-21-C, 2011-02CON-06-C), and written in-
formed consent was obtained from all subjects or their parents.
Data sharing and collaboration
There are no linked research data sets for this paper. Data will be
made available on request.
Provenance and peer review
This article has undergone peer review.
Appendix A. Supplementary data
Supplementary material related to this article can be found, in the
online version, at doi:https://doi.org/10.1016/j.maturitas.2020.01.003.
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