Osteoporos IntDOI 10.1007/s00198-008-0573-7
Additive benefit of higher testosterone levels and vitamin Dplus calcium supplementation in regard to fall riskreduction among older men and women
H. A. Bischoff-Ferrari & E. J. Orav & B. Dawson-Hughes
Received: 28 September 2007 / Accepted: 3 December 2007
# International Osteoporosis Foundation and National Osteoporosis Foundation 2008
uals also took vitD+cal, the fall reduction was enhanced
Summary Higher physiologic testosterone levels among
(men: OR=0.16; 95% CI [0.03,0.90] / women: OR=0.15;
community dwelling older men and women may protect
95% CI [0.04,0.57]). Similarly, women in the top quartile
against falls, and this benefit may be further increased
of dihydroepiandrosterone sulfate (DHEA-S) had a lower
among those taking additional vitamin D plus calcium.
risk of falling (OR =0.39; 95% CI [0.16,0.93]). Other sex
Introduction The aim of this study is to investigate sex
hormones and SHBG did not predict falling in men or
hormone levels and fall risk in older men and women.
Methods One hundred and ninety-nine men and 246
Conclusions Higher testosterone levels in both genders and
women age 65+ living at home were followed for 3 years
higher DHEA-S levels in women predicted a more than 60%
after baseline assessment of sex hormones. Analyses
lower risk of falling. With vitD+cal, the anti-fall benefit of
controlled for several covariates, including baseline 25-
higher physiologic testosterone levels is enhanced from 78%
hydroxyvitamin D, sex hormone binding globulin, and
to 84% among men and from 66% to 85% among women.
vitamin D plus calcium treatment (vitD+cal). Results Compared to the lowest quartile, men and women
Keywords Falls . Older individuals . Sex hormones .
in the highest quartile of total testosterone had a decreased
odds of falling (men: OR=0.22; 95% CI [0.07,0.72]/women: OR=0.34; 95% CI [0.14,0.83]); if those individ-
An inverse association between sex hormone levels and hip
Department of Rheumatology and Institute for Physical Medicine,
fracture risk has been documented [explained by
benefits on bone remodeling and bone density [,
Additionally, lower sex hormone levels may be associated
with increased fall risk as an alternative pathway explainingelevated hip fracture risk with age. Given that falling is a
primary risk factor of hip fracture among older individuals,
Jean Mayer USDA Human Nutrition Research Center on Aging,Tufts University,
factors that relate to falling need careful evaluation,
especially if deficiencies are amendable to treatment.
Testosterone levels decline with age in both men and
women and testosterone replacement may increase lean
Department of Biostatistics, Harvard School of Public Health,Boston, USA
body mass [] and muscle strength [] in men with lowtestosterone levels. Among healthy older men with normal
to mildly decreased testosterone levels, testosterone sup-
strength and functional performance were unchanged with
testosterone replacement in some studies performed in men
day) plus calcium (500 mg per day) on bone mineral
age 65 and older [, Regarding fall risk and
density and fractures Of 848 persons who were
testosterone levels, observational studies have been incon-
prescreened with questionnaires, 545 were invited for
sistent with an inverse association documented in one
screening. The final study sample was 445 subjects (199
of two prospective studies ] among older men. Whether
men and 245 women). Apart from DXA measurements and
higher testosterone levels reduce fall risk among women,
fractures, falls were assessed throughout the trial, as well as
where levels of the hormone are far lower, is unclear ,
sex hormone levels at baseline. The latter data were used in
Bioavailable and free estradiol levels decline with age in
the present analyses. All participants provided written
men and women ]. While some studies found that
informed consent and the study protocol was approved by
estrogen therapy may enhance muscle strength in older
the Investigation Review Board at Tufts University.
women [others did not find a benefit , ]. Limited data from one observational study suggested no
association between estrogen levels and muscle strength orfall risk in older men or women ].
The trial enrolled healthy ambulatory older men and women
DHEA-S exerts its action indirectly after its conversion
age 65 or older living in the community []. The trial
to androgens and estrogens in peripheral tissues. Its
excluded individuals with Parkinson's disease or hemiplegia,
association with falling among older individuals is unclear
cancer or hyperparathyroidism. The criteria of exclusion also
with two observational studies suggesting a positive
included a kidney stone in the past 5 years, renal disease
correlation of the hormone with muscle strength in older
(serum creatinine >1.2 mg/dl), liver disease, bilateral hip
men and women [Whether sex hormone binding
surgery, dietary calcium intake exceeding 1500 mg/day,
globulin (SHBG) is associated with falling has not been
therapy with testosterone, estrogen, tamoxifen, bisphospho-
explored. However, SHBG may play an important adverse
nate, fluoride or calcitonin in the past two years.
role in older individuals as it increases with age andpossibly contributes to a decreased bioavailability of sex
Given the scarcity of studies on the role of sex hormone
Of 445 subjects who were randomized, 389 attended the 3-
levels and the risk of falling in older persons, we assess the
year follow-up visit and 318 were still on study medication
association of baseline sex hormone levels and subsequent
at the 3-year follow-up visit. For this analysis, we used all
risk of falling over a 3-year follow-up. Taking advantage of
the blinded intervention with vitamin D plus calcium withinthis data set, we were able to explore a possible additive
benefit of higher hormone levels and treatment withvitamin D plus calcium. Vitamin D, similar to testosterone
Falls were ascertained by postcards. Participants were asked
and estrogen, is a steroid hormone, and previous random-
to send a postcard after every fall, which was then followed
ized controlled trials suggested a significant improvement
by a phone call from a staff member to assess the
of strength ] and reduction of falls –with vitamin
circumstances of the fall. In addition, falls were ascertained
D treatment. In the same data set, vitamin D plus calcium
significantly reduced the odds of falling in women (odds
We included all reported fall events. Falls were defined
ratio [OR], 0.54; 95% confidence interval [CI], 0.30–0.97),
as “unintentionally coming to rest on the ground, floor, or
but not in men (OR, 0.93; 95% CI, 0.50–1.72) [If there
other lower level” [Falls due to severe trauma
was an additive benefit, future intervention studies targeting
involving external force or vehicles were not counted as a
falls may optimize sex hormone levels and vitamin D plus
fall. Falling at least once was the primary outcome of the
calcium intake to decrease fall risk most efficiently. Finally,
we studied the association of sex hormone levels with totaland leg lean body mass.
Baseline BMI is weight in kilograms divided by height in
meters squared measured at the study center. Physicalactivity included leisure, household, and occupational
activity as estimated by the Physical Activity Scale for theElderly (PASE) questionnaire ]. Tobacco use and use of
The Boston Stop-It trial is a 3-year double-blind random-
alcoholic beverages were assessed by a questionnaire at
ized controlled trial on the effect of vitamin D3 (700 IU per
Comorbid conditions assessed at baseline with a ques-
8.6%, respectively. Total testosterone was measured in serum
tionnaire were summarized with a comorbidity score, which
using radioimmunoassay kits from Diagnostic Products Corp
represents the sum of the following comorbid conditions:
(Los Angeles, CA). There are no significant cross-reactions
diabetes, hyperthyroidism, hypertension, cancer, low back
with other natural steroids. The intra- and inter-assay CVs
surgery, previous hip fracture, and stomach surgery.
were 5.9% and 8.7%, respectively. Free testosterone was
Total and leg lean body mass was measured by dual-
measured by the method of Hammond et al. The
energy x-ray absorptiometry using a DPX-L scanner (Lunar
measurement was done with centrifugal ultrafiltration and
Radiation, Madison Wisconsin). The reproducibility of lean
the inter- and intra-assay CVs are 8.9% and 5.2%,
tissue mass measurements was 1.0% ].
On the baseline visit, venous blood was collected between
We used logistic regression to evaluate the effect of quartiles
7:00 and 9:30 a.m. after the subjects had fasted for at least
of sex hormone levels with the lowest quartile as the
8 hours. Plasma 25-OHD levels were measured by
reference on a person’s risk of falling at least once during
competitive protein binding assay, as described by Preece
the 3-year follow-up. In men and women, all analyses were
et al., with intra- and interassay CVs of 5.6% to 7.7% ].
controlled for age in years, baseline BMI in kg/m2 (<25, 25–
All following hormones were measured in the laboratory of
29, ≥30), baseline plasma 25-OHD levels, baseline PASE
the late Dr. Christopher Longcope at the University of
status for physical activity assessment, baseline smoking
Massachusetts in Worcester. Estrone and estradiol were
status (never, current, former smoker), baseline use of
measured in serum by radioimmunoassay following solvent
alcoholic beverages (yes/no), baseline number of comorbid
extraction and celite chromatography. The intra- and inter-
conditions, treatment with vitamin D plus calcium or
assay CVs for estrone were 5.0 and 10.0% and for estradiol
placebo, and length of follow-up in days. The analyses for
were 7.0 and 13.2%, respectively. The estradiol assay had a
total testosterone, estrone and estradiol were also controlled
detection level of 5 to 7 pg/ml. Androstenedione was
measured in serum using radioimmunoassay kits from
In addition, we compared the baseline mean total lean
Diagnostic System Laboratories (Webster, TX). This anti-
body mass and the baseline mean leg lean body mass
body is highly specific with negligible cross-reaction with
among quartiles of baseline sex hormone levels using a
other steroids. The intra- and inter-assay CVs were 7.3%
multiple linear regression model while adjusting for age in
and 9.8%, respectively. DHEA-S was measured in serum
years, baseline BMI in kg/m2 (<25, 25–29, ≥30), baseline
using radioimmunoassay kits from ICN Biomedical (Costa-
plasma 25-OHD levels, baseline PASE, baseline smoking
Mesa, CA) with relatively high cross-reactions, 30%–60%,
status (never, current, former smoker), baseline use of
with dehydroepiandrosterone and androstenedione. Since
alcoholic beverages (yes/no) and baseline number of
DHEA-S circulates at levels at least 1,000 times those of the
comorbid conditions. Least square means were used to
other two steroids, this cross-reaction does not interfere with
express the adjusted mean and percent difference in lean
the assay. The intra- and inter-assay CVs were 4.3% and
body mass by quartiles of sex hormone levels.
Table 1 Characteristics of thestudy population
All analyses were conducted with SAS (Version 8.2; SAS
in the highest quartile of total testosterone with serum
Institute Inc., Cary, NC, USA). All p-values were two-sided.
levels of 5.68 ng/ml or above had a 78% decreased odds offalling compared to men in the lowest quartile with totaltestosterone levels of 3.77 ng/ml or less (OR=0.22; 95% CI
[0.07,0.72]). There was a significant trend between a lowerodds of falling and higher total testosterone levels (p=
Baseline characteristics by sex are displayed in Table
0.005). See Fig. for exact boundaries of quartiles and
While mean age was the same for men and women, women
were less physically active, had lower 25-hydroxyvitamin
Among women, similar to men, there was a significant
D levels and were less likely to be ever smokers. Hormone
trend between a lower odds of falling and higher testosterone
levels, differed by sex significantly with one exception,
levels (p=0.03). Women in the top quartile of testosterone
estrone. Overall, 49% (97) of men and 57% (134) of
with serum levels of 0.49 ng/ml and above had a 66%
women fell during the 3-year follow-up.
decreased risk of falling compared to those in the lowestquartile with serum levels of 0.20 ng/ml or less (OR=0.34;
95% CI [0.14,0.83]). See Fig. for exact boundaries ofquartiles and illustration of the observed trend.
Among men, total testosterone levels independent of SHBG
Also, women in the top quartile of DHEA-S had a 61%
were significantly associated with the odds of falling. Men
lower risk of falling compared to those in the lowest
OR (95% CI) 0.75 Quartiles of total testosterone OR (95% CI) 0.75 Quartiles of total testosterone
Fig. 1 Odds of falling by quartile of total testosterone in men and in
women (test for trend: p=0.03) suggesting a decrease in the odds of
women. Independent of age, body mass index, physical activity,
falling with higher testosterone levels. In a comparison of the two
SHBG levels, 25(OH)D levels, vitamin D plus calcium treatment,
extreme quartiles, men in the highest quartile had a 78% and women
number of comorbid conditions, smoking and alcohol consumption,
had a 66% lower odds of falling. Results were similar with or without
there was a significant trend in men (test for trend: p=0.005) and
quartile (OR=0.39; 95% CI [0.16,0.93] (see Table There
vitamin D plus calcium supplementation on fall prevention in
appeared to be a threshold effect with a benefit in all
Table Among men and women, there was an additional
women reaching serum levels of above 0.30 μg/ml, the
benefit of being in the sex-specific top quartile of serum
upper end of the lowest quartile. Among men, there was a
testosterone plus being randomized to vitamin D and calcium.
similar directionality with a decreased risk of falling withhigher DHEA-S levels. However, this was not significant.
Estrone, estradiol, free testosterone, androstenedione,
and SHBG were not significantly associated with the odds
There was a significant inverse association between
baseline total and leg lean body mass, and quartiles of
As this was a double-blind RCT with vitamin D plus
SHBG in both men and women (see adjusted means in
calcium compared to placebo ], we were able to explore a
Fig. and b). All sex hormones were not appreciably
possible additive benefit of higher testosterone levels and
Table 2 Odds of falling across quartiles of estradiol, DHEA-S, and SHBG
Effect women OR [95% CI] p-value for trend
All analyses controlled for age, baseline BMI, baseline plasma 25-OHD levels, baseline PASE status for physical activity assessment, baselinesmoking status, baseline use of alcoholic beverages, baseline number of comorbid conditions, treatment with vitamin D plus calcium or placebo,and length of follow-up in days. Similar to estrone, there was no significant association between the odds of falling and estradiol andandrostenedione levels*p-value for trend test. **Significantly different from reference
Table 3 Effect of higher testosterone levels on falling by vitamin D + calcium supplementation
Sex-specific total testosterone quartiles
All analyses controlled for age, baseline BMI, baseline plasma 25-OHD levels, baseline PASE status for physical activity assessment, baseline smokingstatus, baseline use of alcoholic beverages, baseline number of comorbid conditions, and length of follow-up in days. Our data suggest an additivebenefit of high testosterone levels and vitamin D (700 IU per day) plus calcium (500 mg per day) supplementation in older men and women
density in men ] and women ], higher estrogen levelsmay not protect from falls in either sex.
We found that fall risk declines with higher physiological
We found that higher DHEA-S levels may reduce the
testosterone levels among older ambulatory men and
odds of falling by 61% in women and there appeared to be
women independent of age, SHBG levels, body mass
a similar direction in men. Our study adds to the literature
index, physical activity, smoking, alcohol consumption,
suggesting that higher physiological levels, above 0.31 μg/l,
number of comorbid conditions, vitamin D plus calciumtreatment, and length of follow-up. Men and women in thetop quartile of sex specific testosterone levels had a 78%
respectively 66% lower risk of falling compared to
individuals in the lowest quartile. This benefit was
augmented if individuals in the top quartile had additional
vitamin D plus calcium supplementation. In this subgroup
fall risk was reduced by 84% in men and 85% in women.
The additional benefit of vitamin D plus calcium may be
explained by evidence from several randomized controlled
trials showing that vitamin D supplementation reduces the
adjusted leg lean mass (SE)
risk of falls in older individuals by enhancing muscle
strength and balance , , , From a clinical
perspective the possible additive benefit of higher physio-
Quartiles of SHBG
logic testosterone levels and vitamin D plus calcium
supplementation is of interest as the additional benefit
appears to be significant, applies to both sexes, and both
*
components can be altered by treatment. In fact, in our
earlier analyses of the RCT, which did not take testosterone
levels into consideration, vitamin D plus calcium reduced
falls among women (OR =0.54; 95% confidence interval
[CI], 0.30–0.97), but not in men (OR=0.93; 95% CI, 0.50–
*
1.72) compared to placebo ]. Thus, especially among
men, the additional correction of testosterone levels to theupper end of the physiologic range may be important. Adjusted lean total body mass (SE)
There was no association between estrogen levels and
falls in either sex. Our findings are consistent with two
Quartiles of SHBG
prospective cohort studies, which did not find an associa-
Fig. 2 a Adjusted mean baseline leg. b Total body lean mass byquartiles of baseline SHBG. Mean adjusted lean mass by quartiles of
tion between estrogen levels and incident falls among older
SHBG is adjusted for age, physical activity, 25(OH)D levels, number
men ] or women ]. Furthermore, one double-
of comorbid conditions, smoking and alcohol consumption. P-values
blind randomized controlled trial with falls as the outcome
for comparison of quartiles with reference quartile (bottom quartile for
did not find a protective effect of hormone replacement
SHBG): *<0.05, **<0.001. Among men, the test for trend wassignificant for total body (p=0.005) and leg (0.03) lean mass. Among
therapy in ambulatory older women [Thus, in contrast
women, the test for trend was significant among women for total body
to the previously documented benefit of estrogen on bone
may be beneficial for fall prevention in women. Additional
levels, as this may be sufficient for fall prevention
data are needed in both men and women.
according to our results. The combined benefit of higher
There was no association of the directly measured free
testosterone and vitamin D plus calcium appears to be
testosterone on falls in both genders. Physiologically, it is
expected that free testosterone reflects the bioavailable part
Based on our cross-sectional findings, body composition
of total testosterone that enters the cells and is most
is not associated with sex hormones but SHBG levels. Lean
sensitive to outcomes, such as falls. However, it has been
mass was highest among men and women with low SHBG
suggested that measurement of free testosterone may
levels. Thus, factors that impact on SHBG status may need
present with difficulties or may not best represent the
bioavailable fraction of testosterone ]. Alternatively, wecontrolled for SHBG when assessing the benefits oftestosterone, which may approximates the truly bioavailable
fraction of testosterone. Androstenedione levels and SHBGlevels were not associated with falling in men or women.
Only SHBG showed a significant inverse association
with total and leg lean body mass in men and women. Specifically, based on our adjusted results, men in the topquartile of serum SHBG concentrations had a 6% lower leg
This study was supported by a grant from the
lean mass and women in the top quartile had a 9% lower
Charles H. Farnsworth Trust, Boston, Mass (US Trust Company,trustee), and by grant AG10353 from the National Institutes of Health,
leg lean mass. Higher SHGB levels have previously been
Bethesda, Md, and a Swiss National Foundation Professorship Grant.
identified as a risk factor for hip fractures in the Study of
Role of the Sponsors: No sponsors participated in the design and
Osteoporotic Fracture (SOF) [Our results support these
conduct of the study; in the collection, analysis, and interpretation of
findings indirectly, as low leg lean body mass is a correlate
the data; or in the preparation, review, or approval of the manuscript.
of quadriceps weakness [and poor structural parametersof bone [which are risk factors for hip fractures ]. However, leg lean mass is a surrogate of muscle force with
limitations and direct strength measures are preferable if thetarget endpoint is falling. Mechanistically, a higher protein
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WORKFORCE SOLUTIONS Case Study - Unemployment Cost ManagementExelon Corporation is one of the nation’s largest electric utilities with more than $15 billion in annual revenues, and Exelon Corporation is one of the nation’s largest electric utilities with more than $15 billion in annual revenues. It distributes electricity to approximately 5.2 million customers in Illinois and Pennsylvan
Before we speak about infertility, it is important to define the word. Many of my patients believe that if they do not conceive on their first try, they will never get pregnant. This is so untrue. Infertility is defined as a lack of conception after 12 months of trying without birth control and with frequent intercourse in a woman under the age of 35, and after 6 months in a woman over age 35.