MUSCLE-BONE INTERACTIONS ACROSS AGE IN MEN
Department of Health and Exercise Science, University of Oklahoma, Norman,
06 October 2005
Journal of Sports Science and Medicine (2006) 5, 43
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study examined the relationship of muscular strength and lean tissue
with age-related patterns in bone mineral density (BMD) in men 20-81
years of age. Subjects were assigned to one of three age groups, Young
Men (YM), (n = 25, 20-39 yrs), Middle-aged Men (MM) (n = 24, 40-59
yrs), and Older Men (OM) (n = 23, 60-81 yrs). Isotonic and isokinetic
strength was assessed for the quadriceps and hamstrings muscle groups.
DXA (Lunar DPX-IQ) was used to measure spine, hip, and total body
BMD and body composition. OM had significantly lower (p < 0.05)
total lean body mass (LBM) than MM and lower leg lean mass (LM) than
YM and MM. OM had significantly lower (p < 0.01) BMD than YM and
MM at the femoral neck and total hip sites and a higher proportion
of OM were osteopenic and osteoporotic at the total hip site. Isotonic
and isokinetic strength for both muscle groups was positively related
(p < 0.05) with the hip BMD sites (r = 0.38-.67). Leg LM also was
positively related to hip BMD (r = 0.37-.58). Multiple Regression
analyses determined that age and lean mass (LBM or leg LM) were significant
predictors (p < 0.05) of femoral neck, and total hip BMD, while
lean mass (LBM or leg LM) was a significant predictor (p < 0.05)
of BMD at the spine and trochanter sites. Isotonic and isokinetic
leg strength variables were significant predictors (p < 0.05) of
the total body, total hip and trochanter BMD. In conclusion, leg strength,
leg LM, and total LBM were significant predictors of BMD in men, independent
of age. These findings emphasize the importance of maintaining lean
body mass for the bone health of aging men.
WORDS: Lean body mass, osteopenia, osteoporosis, muscle strength,
Osteoporosis has been viewed primarily as a health issue for postmenopausal
women, however, about 20% of all hip fractures occur in men and
vertebral fractures may be as common in men as in women (Melton,
Writing Group for the ISCD Position Development Conference, 2004).
The male lifetime risk of any fracture of the hip, spine, or distal
forearm is 13%, which is similar to the lifetime risk of prostate
cancer (Melton, 1999).
Osteoporosis may account for 60-85% of hip fractures in men and
70-90% of vertebral fractures, thus there is a relationship between
low bone mineral density (BMD) and fracture risk in men (Melton,
Ballard et al., 2003
reported that 71% of the elderly Caucasian men (65-93 years) in
their study were osteopenic at the femoral neck and 9.8 % osteoporotic;
whereas these prevalences were lower for the spine (25.5% and 7.8%).
Taaffe et al., 2003
also determined that 7.8% of their Caucasian male population (ages
70-79 years) were osteoporotic at the femoral neck BMD site.
It is well known that mechanical loading of the skeleton via gravitational
forces or forces produced by muscular contraction will influence
bone mass (Frost, 1997;
Turner and Robling, 2003).
The changes in bone mass with aging generally follow the age-related
changes in muscle strength. Since the bone adapts to alterations
in mechanical loading associated with muscle function (Frost, 1997),
measurements of muscle strength, muscle mass, and bone mass may
be useful indicators of the contribution of muscle to bone
strength. Body weight, comprised of fat mass (FM) and lean body
mass (LBM), contributes to gravitational forces on the skeleton,
while lean body mass contributes an additional component of force
through muscle contraction. As a person ages, body composition changes
resulting in losses in bone mass and lean mass and increases in
FM (Hameed et al., 2002).
Recently, it was reported that men aged 85+ years had significantly
lower body weight and lean mass than men 65-69 years of age (Ballard
et al., 2003).
Several studies have examined the relative contribution of FM and
LBM to BMD in the aging population (Kenny et al., 2000;
Ravaglia et al., 2000;
Taaffe et al., 2001).
Bone-free LBM, not FM, has been determined to be a significant contributor
to BMD (Ravaglia et al., 2000;
Taaffe et al., 2001).
Taaffe et al., 2003
examined physical performance of the lower extremities and its relationship
with hip BMD. They found that the strongest relationship between
physical performance and hip BMD was located at the trochanter.
Men with the poorest walking endurance were 2.78 times more likely
to have osteoporosis at the hip, supporting the site-specific effects
of mechanical loading.
There have been few studies investigating the bone status of adult
men across the lifespan, including the years when peak bone mass
is attained. The purpose of this study was to examine the influence
of muscular strength and body composition on age-related BMD patterns
in apparently healthy, sedentary men, 20- 81 years of age. It was
hypothesized that decreases in spine BMD would be evident by middle-age
(40- 59 years) whereas the hip BMD would decline in the older age
group (60-81 years). We expected that muscle mass and strength would
be significant predictors of BMD independent of age for men.
Seventy-two apparently healthy, sedentary men, 20 - 81 years of
age, volunteered to participate in this study. All subjects were
selected on the criterion that they had not engaged in a habitual
exercise program within the previous year. Subjects were assigned
to one of three age groups, Young Men 20-39 years (YM, n = 25),
Middle-aged Men 40-59 years (MM, n = 24), or Older Men 60-81 years
(OM, n = 23). These age categories were chosen to correspond with
the expected age related decline in BMD at the spine and hip, which
begins around 40 years at the spine and 60-65 years at the hip (Writing
Group for the ISCD Position Development Conference, 2004).
Participants completed the PAR- Q, the Godin Leisure-Time Questionnaire,
and a medical history questionnaire prior to testing. The Godin
Leisure-Time Questionnaire determined the number of times per week
subjects performed mild or minimal effort activities (i.e, yoga,
archery, bowling, etc.), moderate, not exhausting activities (i.e.,
fast walking, tennis, badminton, popular and folk dancing, etc.)
and strenuous activities (heart beats rapidly) (i.e., running, football,
soccer, vigorous swimming, etc.). Subjects, 60 years of age and
older, obtained medical clearance from their personal physicians
prior to participation in the study. All subjects signed a written
informed consent. Exclusion criteria were: 1. current use of medications
that affect bone density (e.g., thiazide diuretics, testosterone,
calcitonin, chemo-therapeutics, corticosteroids, or anticonvulsants);
2. medical conditions that affect bone density (e.g., hypogonadism,
thyroid disease, epilepsy, diabetes, kidney stones); 3. current
smokers; and 4. participation in endurance or resistance training
within the previous year. The University of Oklahoma Institutional
Review Board approved all procedures for this study.
density and body composition assessments
BMD (g·cm-2) of the total body, AP lumbar spine (L2-L4),
and the left proximal femur (femoral neck, trochanter, and total
hip) was assessed by Dual Energy X-Ray Absorptiometry (DXA; GE Lunar
DPX-IQ, software version 4.7b). Body composition variables, fat
mass (FM), total body bone-free lean mass (LBM), and left leg bone-free
lean mass (leg LM), were determined from the total body DXA scan.
One qualified technician performed all scan analyses. Quality assurance
procedures were performed daily for calibration prior to each scanning
session. In vivo precision for the proximal femur, spine and total
body are < 1%. In vitro precision and accuracy for the
spine phantom are 0.6% and 0.8%, respectively. The prevalence of
osteoporosis and osteopenia was estimated based on the WHO classifications
(normal, T-score > -1.0; osteopenia, T-score -1.1 to -2.4;
and osteoporosis, T- score < -2.5) using the male reference
database (Writing Group for the ISCD Position Development Conference,
The quadriceps (knee extension) and hamstring (knee flexion) muscle
groups of the right leg were tested for isotonic and isokinetic
strength according to the standardized procedures in the neuromuscular
laboratory. Isotonic strength assessment consisted of a one-repetition
maximum (1-RM) protocol for each muscle group using Cybex®
equipment. 1-RMs were obtained within 5 trials after an adequate
and one minute of rest between trials. Isokinetic strength (peak
torque, PT), at three contraction speeds, 60°·s-1,
was assessed using a Biodex® dynamometer. Chair and dynamometer
adjustments were made individually to maintain proper joint angles
with the dynamometer. The subject was secured in the chair by a
waist belt, chest belts, and a leg belt to ensure isolation of the
involved muscle groups. Each contraction speed began with several
practice trials, followed by three maximal repetitions (extension
and flexion) performed consecutively. The practice trials and the
three contraction speeds each were separated by a one minute rest
period. PT was determined as the highest torque value obtained from
the three trials. The day to day intraclass correlation coefficients
were 0.80 - 0.99 for isokinetic strength measures and 0.95 - 0.
98 for isotonic strength measures.
All data are reported as means ± standard error (SE). SPSS Version
11.5 was used to analyze the data. Descriptive statistics were computed
for the dependent variables. One way analysis of variance was used
to detect age group differences in BMD and body composition variables.
The Bonferroni post hoc multiple comparison procedure was used to
determine the source of significant differences when a significant
age group effect was found. Chi-square analysis was performed to
detect associations between age group and the prevalence of osteopenia
and osteoporosis for the spine and total hip BMD sites. Pearson's
Zero-order Correlation Coefficients were computed to determine relationships
of muscular strength and body composition variables with BMD variables.
Stepwise Multiple Regression was used to determine whether age and
body composition variables (FM, LBM or leg LM) were significant
predictors of BMD. Additional Stepwise Multiple Regression analyses
were used to determine whether age and isotonic leg strength (quadriceps
1-RM, hamstrings 1-RM) or age and isokinetic leg strength (quadriceps
PT, hamstrings PT at 60, 180, and 240°·s-1) were significant
predictors of BMD. The level of significance was set at p <
physical characteristics of the three age groups are shown in Table
1. The older men had significantly (p < 0.05) lower BMI (kg·m-2)
and LBM (kg) than the middle-aged men. The older men had significantly
(p < 0.05) lower leg LM (kg) than both the young men and middle-aged
men. Although not statistically significant, there was a trend for
an age group effect for body weight (p = 0.063), with the older
men being 12.1 kg lighter than middle-aged men. There were no significant
(p > 0.05) differences in height, fat mass, or physical activity
scores between the three age groups.
The age group comparisons for BMD are shown in Table
2. There were no significant (p > 0.05) age differences at
the spine or total body sites, however older men had significantly
(p < 0.05) lower BMD at the femoral neck and the total hip sites
compared to both the young and middle-aged groups. Percent differences
in age group means for each BMD site are shown in Figure
1. The older men were 14.5% lower than the middle-aged men and
were 20.7% lower than the younger men at the femoral neck. Likewise,
the older men were 13.4% (vs. middle-aged) and 14.2% (vs. younger)
lower at the total hip. The prevalence of osteopenia and osteoporosis
at the spine and total hip for each age group is shown in Table
3. T-scores in the range for osteopenia were observed for each
age group for the spine and total hip sites. Chi-square analyses
detected a significant association (p = 0.012) between age groups
and the prevalence of osteopenia at the total hip as a higher percentage
(39%) of older men had osteopenia than the young men (8%) and middle
aged men (17%) at this BMD site. A small proportion of middle-aged
and older men had T-scores < -2.5 for the spine site.
Correlation coefficients between isokinetic and isotonic strength
with BMD are shown in Table 4.
Generally, leg strength showed significant moderate positive relationships
with hip BMD. Both quadriceps and hamstring strength was related
with hip BMD variables, with the strongest correlations found between
the quadriceps and the femoral neck (ranging from r = 0.62 to 0.67).
to moderate positive correlations were found between lean mass variables
(LBM, leg LM) and the BMD measures. Significant (p < 0.05) correlation
coefficients were found between LBM and the hip BMD sites (r = 0.59
total hip, r = 0.50 femoral neck, r = 0.42 trochanter). Similar
correlations existed between leg LM and the hip sites (r = 0.58
total hip, r = 0.55 femoral neck, r = 0.37 trochanter). Both LBM
and leg LM were positively related (p < 0.05) to BMD at the total
body (r = 0.41, r = 0.37, respectively) and spine (r = 0.31, r =
0.25, respectively) BMD sites.
Stepwise Multiple Regression analyses were performed to determine
significant body composition and strength predictors of each BMD
site. Since LBM and leg LM were highly correlated (r = 0.96, p <
0.001), these variables were used in two separate regression analyses
(age, FM and LBM or age, FM, and leg LM) (Table
5). The two analyses yielded nearly identical regression results.
FM and age were significant (p < 0.001) predictors for total
body BMD. LBM or Leg LM alone was a significant predictor for spine
(p < 0.05) and trochanter BMD (p < 0.001). LBM or Leg LM and
age were significant predictors (p < 0.001) for the femoral neck
and total hip BMD. In order to assess the contribution of leg strength,
isotonic strength of the quadriceps and hamstrings were used as
independent variables for each BMD site (Table
6). Quadriceps strength and age significantly (p < 0.001)
predicted femoral neck BMD, while quadriceps strength alone significantly
(p < 0.001) predicted total body, trochanter, and total hip BMD.
The contribution of isokinetic leg strength to BMD was evaluated
using the peak torque of the quadriceps and hamstrings at three
different speeds of contraction (60, 180, and 240°·s-1)
as independent variables (Table
7). Quadriceps PT at each speed and
age significantly (p < 0.001) predicted femoral neck BMD, while
quadriceps PT at each speed alone significantly (p < 0.01) predicted
TB BMD. Hamstrings PT and quadriceps PT at 60°.s-1 were
significant (p < 0.001) predictors of total hip BMD, while quadriceps
PT at 180 and 240°·s-1 alone significantly (p < 0.001)
predicted total hip BMD. Hamstrings PT at each speed significantly
(p < 0.001) predicted trochanter BMD.
this cross-sectional study, we examined the relationship of body
composition and muscular strength variables with bone mineral density
in apparently healthy, sedentary men, 20-81 years of age. In contrast
to previous studies (Ballard et al., 2003;
Center et al., 2000;
Kenny et al., 2000;
Ravaglia et al., 2000;
Taaffe et al., 2001;
our subjects were evaluated for isotonic and isokinetic strength
of the knee flexors and extensors. Additionally, most previous studies
focused only on elderly men in their analyses (Ballard et al., 2003;
Kenny et al., 2000;
Taaffe et al., 2001;
whereas this study included a wide age range of 20 - 81 years. Decreased
LBM and leg LM became evident in the older age group (60-81 years),
which coincided with decreased muscle strength for the quadriceps
and hamstrings muscle groups (Runnels et al., 2005).
However, we did not find an age group difference in FM and there
was only a trend for an age group effect for body weight. In a cross-
sectional study of men 65 - 93 years of age, Ballard et al., 2003
reported that as men aged, both body weight and LBM decreased.
Older men, 60-81 years of age, had lower BMD at the femoral neck
and total hip sites compared to both the young (20-39 years), and
(40-59 years) men. However, there were no detectable age group differences
in the spine or total body BMD. The young men in our study had a
surprisingly high prevalence (20%) of low spine bone density. In
a cohort of men 20-80 years of age, Clarke et al., 2002 reported an age-related decline only in the femoral
neck BMD with no age group differences in spine, total body or other
hip sites. There are several possible explanations for differences
in our findings compared to previous studies. Clarke et al., 2002
excluded men reporting a sedentary lifestyle from their study; therefore,
their subjects may have been more physically active than our subjects.
The spine BMD of the older men in our study also may have been influenced
by artifact, such osteoarthritis in the lumbar spine (Melton et
O'Neill and EPOS Group, 2002;
Szulc et al., 2000;
Vallarta-Ast et al., 2002).
Taken together, evidence of young men having lower bone spine BMD
than expected and the possibility of an artificially increased spine
BMD in older men may explain the lack of age-related changes in
The older men exhibited a similar prevalence of osteoporosis as
those reported in previous studies (Ballard et al., 2003;
Taaffe et al., 2003).
Some caution should be used when evaluating BMD T-scores in men,
as the diagnosis of osteoporosis in men is not as definitive as
it is in postmenopausal women. The World Health Organization (1994)
classification compares a patient's BMD to the young adult female
reference population for the diagnosis of osteoporosis and osteopenia
in Caucasian postmenopausal women. However, the application of these
criteria in men as well as the appropriate reference database to
use are controversial (Binkley et al., 2002;
De Laet et al., 2002;
Faulkner and Orwoll, 2002;
O'Neill and EPOS Group, 2002).
The International Society for Clinical Densitometry (2004) recommends
the application of several modifications to the WHO classifications
for the diagnosis of osteoporosis in men.
Regression analysis was used to examine the interactions between
bone mass and total LBM, an indicator of gravitational stress, or
leg LM, which relates to the contractile forces placed upon the
bone. Total LBM and age were significant predictors of femoral neck
and total hip BMD sites (54 and 44% of the variance, respectively).
Total LBM alone was a significant predictor of the spine and trochanter
BMD sites, explaining 8 and 16% of the variance respectively. Regression
analyses using leg LM yielded similar results as those using total
LBM. Leg LM and age were significant predictors of the femoral neck
and total hip BMD sites, explaining 49 and 39% of the variance,
respectively. Leg LM was the only significant predictor of the spine
and trochanter sites (5 and 13% of the variance, respectively).
The standardized regression coefficients indicated that increased
leg LM had a positive effect on BMD, while increased age had a negative
effect on BMD. These results suggest the importance of maintaining
leg LM in aging men. FM and age were entered into the model for
total body BMD, accounting for 20% of the variance. Total body BMD
was the only site influenced by fat tissue, likely due to its contribution
to body weight, and therefore, gravitational stress on the skeleton.
It is well understood that excess forces imposed upon the skeleton
through muscular contraction and/or gravitational loading will result
in increased bone mass. In order to examine the contribution of
muscular contractile forces on hip BMD, separate multiple regression
analyses were performed with isotonic leg strength replacing body
composition as independent variables. Quadriceps strength alone
was entered into the models for the total body, trochanter, and
total hip BMD sites explaining 15, 14, and 41% of the variance,
respectively; whereas both quadriceps strength and age were significant
predictors for the femoral neck site. Therefore, quadriceps strength
and leg LM, independent of age, were influential for the proximal
femur BMD, with each variable accounting for similar proportions
of the variance at these sites. These findings are consistent with
those of Taaffe et al., 2001
who found that LBM was the significant contributor to BMD at the
femoral neck, upper and lower limbs, and for the whole body in men.
Ravaglia et al., 2000
also found significant associations between bone mass and muscle
mass in men 20-95 years of age.
Examination of isokinetic muscle strength in this study offers a
unique approach to determining the contribution of muscular contraction
on BMD. Separate multiple regression analyses using PT strength
of the quadriceps and hamstrings (at 60, 180, and 240°·s-1)
as independent variables, revealed similar results to the isotonic
variables, with PT having a positive influence on BMD. The main
difference between the two types of contraction occurred with the
trochanter BMD regression model. Hamstrings isokinetic strength,
rather than quadriceps, entered the model. At the trochanter, the
hamstrings PT (60, 180, and 240°·s-1) was found to explain
16 - 22% of the variance in BMD, which is slighter higher than that
determined by the isotonic strength of the quadriceps (14%). Hamstring
PT at 60°·s-1 was also entered into the model for the
total hip BMD, which, along with quadriceps PT at 60°·s-1,
accounted for 37% of the variance in BMD. These results strengthen
the argument that muscular contraction has an important influence
on BMD, especially at the hip.
There are several limitations to this study. We did not assess calcium
intake which is an important factor for bone health in men as higher
BMD values have been associated with higher calcium intakes in elderly
men (Ballard et al., 2003;
Nguyen et al., 2000).
For example, Nguyen et al., 2000
reported that men (69.5 ± 6.5 years) in the highest dietary calcium
intake tertile (>710 mg·day-1) exhibited femoral neck
and spine BMD values 5% higher than the men of the lowest tertile
(<460 mg·day-1). However, they also found that the
variation in dietary calcium intake accounted for only 1% of the
total variance in BMD. The average BMD values for our older men
were similar to those reported by Nguyen et al., 2000
for the spine (1.24 ± 0.20) and slightly lower for the femoral neck
(0.92 ± 0.14).
Another limitation is that occupational physical activity data was
not assessed. Leisure time physical activity showed no differences
between the age groups, however this accounts for only a portion
of time spent being physically active during the day. A comprehensive
account of the daily mechanical loading of the skeleton by these
subjects could provide meaningful data in explaining the prevalence
of low bone mass. Generally, physically active individuals of any
age have higher BMD than their sedentary counterparts (Beck and
Another lifestyle factor that can influence bone density is the
incidence of previous fracture, which was not documented in this
study. It has been shown that men without previous fracture have
a higher BMD than those who have fractured at least one time at
some point in their life (Ballard et al., 2003).
60-81years of age, had lower femoral neck and total hip BMD than their
young (20-39 years) and middle-aged (40-59 years) counterparts. Low
bone mass for the spine was exhibited by each age group with prevalence
of osteoporosis evident in the middle-aged and older men. The prevalence
of osteopenia and osteoporosis were greater in the older men at the
total hip site. Regression analyses revealed that total LBM and leg
LM had similar contributions to hip BMD. Isotonic and isokinetic leg
strength and leg lean mass were significant predictors of hip BMD,
independent of age, reinforcing the importance of contractile forces
on bone. Based on our findings, it appears that men as young as 60
years of age should be concerned about bone loss and osteoporosis
risk. Maintenance of lean body mass should be encouraged in aging
men for preservation of bone mass, especially at the hip. The prevention
of osteoporosis is of critical importance for aging men as the life
expectancy of men in the United States is projected to increase.
is an important health problem for men.
mineral density for the hip was lower in older men compared to
their younger and middle-age counterparts. There were age group
differences in the prevalence of osteopenia and osteoporosis for
the total hip BMD site.
strength and bone-free lean body mass were significant predictors
of hip BMD, independent of age, thus reinforcing the importance
of contractile forces on skeletal health.
of muscle mass and strength should be encouraged in aging men
for the reduction of osteoporosis risk.
Ian J. PALMER
Employment: Department of Health and Exercise Science, University
of Oklahoma, Norman OK.
Degree: MS (PhD Candidate).
Research interests: Bone metabolism, exercise interventions,
Eric D. RUNNELS
Employment: Goddard Health Center, University of Oklahoma,
Degree: MS, PT.
Research interests: Neuromuscular function, aging
Employment: Professor, Department of Health and Exercise
Science, University of Oklahoma, Norman OK.
Research interests: Aging, neuromuscular function, resistance
Employment: Associate Professor, Department of Health and
Exercise Science, University of Oklahoma, Norman OK.
Research interests: Bone metabolism, exercise interventions,
bone biomarkers, endocrine responses