Serum Estrogen, But Not Testosterone, Levels Differ between Black and White Men in a Nationally Representative Sample of Americans
- Sabine Rohrmann,
- William G. Nelson,
- Nader Rifai,
- Terry R. Brown,
- Adrian Dobs,
- Norma Kanarek,
- James D. Yager and
- Elizabeth A. Platz
- Author Affiliations
- Division of Cancer Epidemiology (S.R.), German Cancer Research Center, D-69120 Heidelberg, Germany; Departments of Oncology, Pathology, Pharmacology and Molecular Sciences, Radiation Oncology and Molecular Radiation Sciences (W.G.N.); the James Buchanan Brady Urological Institute (W.G.N., E.A.P.); and the Division of Endocrinology and Metabolism (A.D.), Department of Medicine, Johns Hopkins Medical Institutions, Baltimore, Maryland 21205; the Sidney Kimmel Comprehensive Cancer Center (W.G.N., A.D., N.K., J.D.Y., E.A.P.), Baltimore, Maryland 21231; Department of Laboratory Medicine (N.R.), Harvard Medical School and Children’s Hospital, Boston, Massachusetts 02115; and Departments of Biochemistry and Molecular Biology (T.R.B.), Environmental Health Sciences (N.K.), and Epidemiology (E.A.P.) and Division of Toxicology (J.D.Y.), Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland 21205
- Address all correspondence and requests for reprints to: Elizabeth A. Platz, Johns Hopkins Bloomberg School of Public Health, Department of Epidemiology, 615 N. Wolfe St., Rm. E6132, Baltimore, MD 21205. E-mail: eplatz@jhsph.edu.
Abstract
Context: Higher
testosterone in black compared with white men has been postulated to
explain their higher prostate cancer incidence.
Previous studies comparing hormone levels by race
might have been limited by size, restricted age variation, or lack of
representation
of the general population.
Objective: Our objective was to compare serum testosterone, estradiol, and SHBG concentrations among non-Hispanic black, non-Hispanic
white, and Mexican-American men.
Participants, Design, and Setting: A total of 1413 men aged 20+ yr and who attended the morning examination session of the Third National Health and Nutrition
Examination Survey (NHANES III) in 1988–1991 were included in this cross-sectional study.
Measurement: Serum hormone concentrations were measured by electrochemiluminescence immunoassays.
Results: After applying
sampling weights and adjusting for age, percent body fat, alcohol,
smoking, and activity, testosterone concentrations
were not different between non-Hispanic blacks (n =
363; geometric mean, 5.29 ng/ml) and non-Hispanic whites (n = 674; 5.11
ng/ml; P > 0.05) but were higher in Mexican-Americans (n = 376; 5.48 ng/ml; P < 0.05). Non-Hispanic blacks (40.80 pg/ml) had a higher estradiol concentration than non-Hispanic whites (35.46 pg/ml; P < 0.01) and Mexican-Americans (34.11 pg/ml; P < 0.01). Non-Hispanic blacks (36.49 nmol/liter) had a higher SHBG concentration than non-Hispanic whites (34.91 nmol/liter;
P < 0.05) and Mexican-Americans (35.04 nmol/liter; P < 0.05).
Conclusions: Contrary to
the postulated racial difference, testosterone concentrations did not
differ notably between black and white
men. However, blacks had higher estradiol levels.
Mexican-Americans had higher testosterone than whites but similar
estradiol
and SHBG concentrations. Given these findings, it
may be equally if not more important to investigate estradiol as
testosterone
in relation to diseases with racial disparity.
SEX STEROID HORMONES are necessary for
pubertal development and sexual function. They are involved in the
metabolism, accumulation,
and distribution of adipose tissue (1) and in the development and maintenance of the bones (2),
and they may influence the development of common diseases such as type 2
diabetes mellitus, cardiovascular disease, and
osteoporosis. The incidence of these conditions in the
United States varies by race/ethnicity, with Hispanics and blacks
having
a higher prevalence of diabetes (3), blacks having a higher incidence of prostate cancer (4) and mortality from cardiovascular disease (3), and whites having a higher incidence of osteoporosis (5).
Some, but not all, of this variation in disease incidence may be
explained by racial/ethnic differences in the prevalence
of risk factors for these conditions. Indeed,
variation in hormone levels has been hypothesized to contribute to the
racial/ethnic
disparities in the incidence of these important
diseases (6, 7).
Despite long-standing hypotheses that
variation in sex steroid hormone levels contributes to racial
differences in the development
of certain diseases, whether differences between black
and white men in circulating levels of sex steroid hormones exist has
not been investigated across a wide age range in a
large-scale study nationally representative of non-institutionalized
American
men. Furthermore, few studies have examined sex
steroid hormone concentrations in Hispanic men (8, 9). Hispanics are the fastest growing ethnicity in the United States, and they are disproportionately affected by obesity and
diabetes (3).
In a cross-sectional analysis, we investigated serum concentrations of
total testosterone, free testosterone, androstanediol
glucuronide (AAG), estradiol, and SHBG in males of
three major U.S. racial/ethnic groups from early to late adulthood in
the
Third National Health and Nutrition Examination Survey
(NHANES III), a nationally representative sample of
non-institutionalized
Americans.
Subjects and Methods
Study population
Between 1988 and 1994, the National Center for Health Statistics conducted NHANES III (10).
NHANES III was designed as a cross-sectional study using a multistage
stratified, clustered probability sample of the U.S.
civilian non-institutionalized population at
least 2 months old, in which Mexican-Americans, non-Hispanic blacks, and
the
elderly were oversampled. Subjects participated
in an interview and an extensive physical examination. Body height and
weight
and waist circumference were measured during the
medical examination. Cigarette smoking, alcohol consumption, and
physical
activity were assessed using a questionnaire.
Body mass index (BMI) was calculated as weight (kilograms) divided by
the square
of height (meters). We calculated body fat and
percent body fat from bioelectrical impedance analysis, height, weight,
and
age (11).
NHANES III was conducted in two phases
(1988–1991 and 1991–1994). Unbiased national estimates of health and
nutrition characteristics
can be independently produced for each phase.
Within each phase, subjects were randomly assigned to participate in
either
the morning or afternoon/evening examination
session. In total, 33,944 subjects were interviewed in NHANES III, of
which 30,818
had a physical examination. Of the 14,781 males
with an examination, 7772 were at least 20 yr old, of whom 1998
participated
in the morning session of phase I. Morning
sample participants were chosen for this hormone study to reduce
extraneous variation
due to diurnal production of hormones. Serum was
still available for 1470 of these men: 674 non-Hispanic white, 363
non-Hispanic
black, 376 Mexican-American, and 57 other
race/ethnicity. In our analysis of the morning examination session of
phase I, 97.4%
of Mexican-American men were white and 2.6% of
other race. The men of other racial/ethnic groups were excluded because
of
small sample size, leaving 1413 men 20+ yr old
for this analysis.
Hormone measurements
Blood was drawn after an overnight
fast for participants in the morning sample. After centrifugation, the
serum was aliquotted
and stored at −70 C until they were pulled from
the freezers for this project. The serum samples were shipped on dry ice
directly
from the National Center for Health Statistics’
main repository in Atlanta, GA, to the assay laboratory.
Serum concentrations of total
testosterone, AAG, estradiol, and SHBG were measured in the laboratory
of Dr. Nader Rifai at
Children’s Hospital in Boston, MA. Competitive
electrochemiluminescence immunoassays on the 2010 Elecsys autoanalyzer
(Roche
Diagnostics, Indianapolis, IN) were used to
quantify serum testosterone, estradiol, and SHBG. AAG was measured by an
enzyme
immunoassay (Diagnostic Systems Laboratories,
Webster, TX). The participant samples were randomly ordered for testing,
and
the laboratory technicians were blinded to the
identity, age, and race/ethnicity of the participants. The lowest
detection
limits of the assays were as follows:
testosterone, 0.02 ng/ml; estradiol, 5 pg/ml; AAG, 0.33 ng/ml; and SHBG,
3 nmol/liter.
The coefficients of variation for quality
control specimens included during the analyses of the NHANES III
specimens were
as follows: testosterone, 5.9 and 5.8% at 2.5
and 5.5 ng/ml; estradiol, 6.5 and 6.7% at 102.7 and 474.1 pg/ml; AAG,
9.5 and
5.0% at 2.9 and 10.1 ng/ml; and SHBG, 5.3 and
5.9% at 5.3 and 16.6 nmol/liter. In addition, we ran quality control
samples
with a mean estradiol concentration of 39.4
pg/ml, which is in the range of typical male estradiol concentrations;
the interassay
coefficient of variation was 2.5%. Serum
testosterone could not be measured for eight, estradiol for five, AAG
for 16, and
SHBG for seven men. Serum concentrations of
testosterone and estradiol detected in the adult men in NHANES III were
generally
within what is considered as reference values in
adult men in the United States (testosterone, 1.94–8.33 ng/ml;
estradiol,
≤50 pg/ml) (12). We estimated free testosterone concentration from measured testosterone, SHBG, and albumin (available in the NHANES III
public use database) (13).
We selected these hormones for
evaluation for the following reasons: 1) testosterone is the major male
androgen and free testosterone
is a measure of bioavailable testosterone; 2)
AAG is an indicator of the conversion of testosterone to
dihydrotestosterone,
the major intraprostatic androgen; 3) estradiol
is the major estrogen in men; and 4) SHBG is the major carrier of
testosterone
and estradiol in the peripheral circulation.
Statistical analysis
All statistical analyses were performed using SUDAAN (14)
as implemented in SAS version 8.1 (Cary, NC) software. We applied
sampling weights to take into account the specific probabilities
of selection, nonresponse, and differences
between the sample and the total U.S. population (10).
We evaluated racial/ethnic differences in the hormones and SHBG 1)
overall after adjusting for age and 2) within three
age categories reflecting hypothesized hormonal
transitions through life: early adulthood (20–44 yr old), mid-adulthood
(45–69
yr old), and late adulthood (70+ yr old).
Because the serum concentrations were not normally distributed, we
compared geometric
means among the three racial/ethnic groups using
ANOVA. Molar ratios of testosterone to SHBG, estradiol to SHBG, and
testosterone
to estradiol were calculated and analyzed in the
same way.
In linear regression models, we
adjusted for age (1-yr increments), cigarette smoking (never smoker,
former smoker, current
smoker <35 cigarettes/d, current smoker 35+
cigarettes/d), alcohol consumption (never drinker, less than one
drink/wk, one
or more drinks/wk to less than one drink/d, one
or more drinks/d), and physical activity (moderate or vigorous physical
activity
on 0, 1–2, 3–4, 5–6, or ≥7 d/wk), because these
factors may influence hormone concentrations and their prevalence may
vary
by race/ethnicity. We used two measures to
account for adiposity: 1) in one multivariable model we adjusted for BMI
(continuous;
kg/m2), and 2) in a second multivariable model we adjusted for percent body fat (continuous; percent) because BMI itself might
be an indicator of overall body fat but also of muscle mass, especially in younger men (15).
Data on bioelectrical impedance analysis and, thus, percent body fat
were not available for 118 men. All tests were two-sided;
P values < 0.05 were considered to be statistically significant.
The protocols for the conduct of
NHANES III were approved by the Institutional Review Board of the
National Center for Health
Statistics, U.S. Centers for Disease Control and
Prevention. Informed consent was obtained from all participants. The
assay
of these stored serum specimens for sex steroid
hormones was approved by Institutional Review Boards at the Johns
Hopkins
Bloomberg School of Public Health and the
National Center for Health Statistics, U.S. Centers for Disease Control
and Prevention.
Results
Baseline characteristics of the participants by race/ethnicity and age category are shown in Table 1⇓.
Within each age category, median age was comparable between the
racial/ethnic groups. Median BMI and percent body fat were
lowest in the youngest age group, whereas men in
the oldest age group had the highest percent body fat. Mexican-American
men
had the highest percent body fat. Smoking status
tended to differ by age and by race/ethnicity within each age group.
Also,
the frequency of moderate/vigorous physical
activity and alcohol consumption varied by age and by race/ethnicity
within each
age group.
View this table:
TABLE 1.
Characteristics of 1413 male participants, NHANES III (Phase 1), 1988–1991
Differences by race/ethnicity adjusting for age
Circulating total testosterone did not
differ significantly between non-Hispanic black and non-Hispanic white
men after adjusting
for age, BMI or percent body fat, smoking,
alcohol consumption, and physical activity (Table 2⇓).
However, after adjusting for percent body fat, Mexican-American men had
a higher testosterone level than non-Hispanic white
and non-Hispanic black men, although only the
former was significant. Although not different in the age-adjusted
model, Mexican-American
men had a higher estimated free testosterone
concentration than non-Hispanic white men in the multivariable model
when adjusting
for percent body fat. AAG concentration was
higher in non-Hispanic white men than in men of the two other
racial/ethnic groups.
Circulating estradiol was higher in non-Hispanic
black compared with non-Hispanic white and Mexican-American men. SHBG
concentration
was significantly higher in non-Hispanic black
compared with non-Hispanic white men. Mexican-American men had
significantly
lower SHBG concentration than non-Hispanic black
or non-Hispanic white men in the age-adjusted model. In the full model
taking
into account percent body fat, circulating SHBG
concentration in Mexican-American men did not differ significantly from
men
in the other two racial/ethnic groups.
View this table:
TABLE 2.
Serum concentrations of sex steroid hormones and SHBG by race/ethnicity, men 20+ yr old, NHANES III (Phase 1), 1988–1991
Mexican-American men had a higher
circulating testosterone/SHBG molar ratio than non-Hispanic white and
non-Hispanic black
men, although only the former was significant in
the multivariable models. The estradiol/SHBG ratio was significantly
higher
in non-Hispanic black than non-Hispanic white or
Mexican-American men. Non-Hispanic black men had the highest
estradiol/testosterone
ratio, followed by non-Hispanic white and
Mexican-American men.
Differences by race/ethnicity within age groups
Presented in Table 3⇓
are multivariable-adjusted geometric mean hormone concentrations. We
show the results adjusted for percent body fat instead
of BMI because it appeared to account better for
the known inverse correlation between SHBG concentration and adiposity (16). In young adult men (20–44 yr old), total testosterone concentration was significantly lower in non-Hispanic white than
in Mexican-American men (Table 3⇓).
In older men (70+ yr old), non-Hispanic black men had the lowest
circulating testosterone concentration, which differed
significantly from Mexican-American men. No
racial/ethnic differences in circulating total testosterone were
observed in middle-aged
men (45–69 yr old). In young adult men,
Mexican-Americans had significantly higher free testosterone
concentrations than non-Hispanic
white men; in older Mexican-American men, free
testosterone concentrations were significantly higher than in the other
two
racial groups. Young non-Hispanic white men had
significantly higher serum AAG concentrations than non-Hispanic black
and
Mexican-American young men, but no significant
differences were seen in other age groups. At all ages, non-Hispanic
black
men had higher estradiol concentrations than
non-Hispanic whites and Mexican-Americans; this difference was
significant in
the young and middle-aged groups. Circulating
SHBG did not differ between racial/ethnic groups with the exception of a
higher
concentration in older non-Hispanic whites
compared with non-Hispanic blacks. Young adult Mexican-Americans had a
significantly
higher molar testosterone/SHBG ratio than
non-Hispanic white or non-Hispanic black men. This was also seen for
older but not
middle-aged men. Young adult, middle-aged, and
older non-Hispanic black men had higher molar estradiol/SHBG ratios than
non-Hispanic
white and Mexican-American men, although the
differences were not always statistically significant. Similarly, we
noted the
highest estradiol/testosterone ratio in young
adult and older non-Hispanic black men compared with non-Hispanic white
and
Mexican-American men.
View this table:
TABLE 3.
Serum concentrations of sex steroid hormones and SHBG by race/ethnicity within age strata, NHANES III (Phase 1), 1988–1991
Discussion
This is the first cross-sectional study
of racial and ethnic variation in circulating sex steroid hormone and
SHBG concentrations
in a representative sample of adult U.S. men. There
was no significant difference in circulating concentrations of
testosterone
or free testosterone concentrations between
non-Hispanic black and white men overall, but Mexican-American men had
higher
levels than non-Hispanic white men. However,
non-Hispanic black men had the highest estradiol level overall and
across all
ages, which was not explained by racial differences
in the prevalence of factors that influence hormone levels.
We cannot confirm observations of a difference in circulating testosterone concentration between African-American and Caucasian
men as reported previously in some studies (6, 9, 17, 18), including in young men (6, 9, 17).
Differences between our results and the results of previous studies
comparing circulating total testosterone concentrations
between racial groups might be due to differences
in age variation or in sample size or due to lack of representation of
the
general population. In our analysis, serum
testosterone concentration was similar in young non-Hispanic white and
non-Hispanic
black men, which has also been reported in three
U.S. cross-sectional studies (19, 20, 21). In a U.S. longitudinal study, testosterone concentration was higher in young black than white men after adjustment for
age and BMI (22).
However, after further adjustment for waist circumference, there was no
difference between non-Hispanic white and non-Hispanic
black men. In our study, non-Hispanic black and
non-Hispanic white men did not differ notably on their extent of
adiposity.
Thus, the results did not change after we adjusted
for waist circumference in addition to BMI (data not shown) or after we
adjusted for percent body fat instead in the
regression models. A recent review concluded that high circulating
testosterone
concentrations are associated with a lower risk of
type 2 diabetes in men (23). Although several cross-sectional studies reported that men with low testosterone levels have an increased risk of coronary
artery disease, this association is not clearly seen in prospective studies (24).
Testosterone is important for prostate development and function and is a
target for treatment of metastatic prostate cancer,
yet results from epidemiological studies that
examined the association between total and bioavailable testosterone and
prostate
cancer have been inconclusive (25, 26, 27).
Our study provides little evidence for the hypothesis that racial
variation in testosterone and free testosterone accounts,
in part, for the higher risk of prostate cancer in
African-American men, at least as measured by circulating levels.
AAG concentration is commonly used in
epidemiological studies as an indirect measure of 5α-reductase activity
and, thus, the
conversion of testosterone to dihydrotestosterone.
Serum AAG concentration was significantly higher in non-Hispanic whites
than in men of the other two racial/ethnic groups.
This was observed overall and in the different age groups. Higher AAG in
white compared with black men has been seen in
other studies in middle-aged (8, 28) and in elderly (29) but not in young adult men (30).
A lower AAG concentration in non-Hispanic black than white men is not
compatible with the hypothesis that a greater 5α-reductase
activity could be associated with the increased
risk of prostate cancer in African-American men based on a meta-analysis
that
reported an increased risk of prostate cancer with
higher circulating AAG concentration (31). Lower AAG might result in men who have a lower conversion of dihydrotestosterone to 3α-androstanediol or, alternatively,
a higher reconversion of 3α-androstanediol to dihydrotestosterone (32).
However, not much is yet known about racial variation in the activity
of the enzymes that catalyze these conversions. Second,
lower AAG could result in men with a greater
efficiency of conversion of testosterone to estradiol via higher
aromatase activity.
Polymorphisms in the CYP19 gene, which encodes
aromatase, have been reported. However, plasma concentration of total
testosterone,
AAG, and SHBG did not differ by genotype in a
Caucasian population (33). Racial variation in CYP19 alleles has been observed in women (34), but to our knowledge, no study has been published with respect to differences in hormone concentrations in men for most
of these CYP19 polymorphisms.
We observed higher serum estradiol
concentrations and higher estradiol/SHBG ratios in non-Hispanic black
than in non-Hispanic
white or Mexican-American men, a difference that
was pronounced in young and mid-adulthood. Previous studies aside from
one
small study of young men (35) did not report differences in circulating estradiol concentrations between African-Americans and Caucasians in young (6, 17, 20), middle-aged (28), or older men (18). It has been hypothesized that higher estradiol concentrations in African-American men might contribute to higher bone mass
and, thus, lower fracture risk (7) because estradiol inhibits bone resorption (36). The role of estrogens in the development and progression of prostate cancer, which is more common among African-American
than Caucasian or Hispanic men (4),
is not clear. In the Physicians’ Health Study, an inverse association
between circulating estradiol concentration and prostate
cancer was observed after taking testosterone and
SHBG concentrations into account statistically (37), whereas other studies did not report statistically significant positive or inverse associations (25).
SHBG transports sex steroid hormones in
the circulation and, along with albumin, is a determinant of
bioavailable testosterone
and estradiol. It mediates steroid hormone signal
transduction at the plasma membrane, which allows steroid hormones to
act
without entering the cell by interacting with SHBG
membrane receptors (38).
SHBG concentration was lower in Mexican-American than non-Hispanic
white and non-Hispanic black men in the age-adjusted
model; however, the differences were attenuated
after taking into account all covariates, particularly percent body fat.
The
attenuation of the racial/ethnic differences in the
multivariable model is explained by SHBG concentration being inversely
associated with body fat (16)
and the higher percentage of body fat in Mexican-Americans compared
with either of the other two racial/ethnic groups. SHBG
concentrations were similar in non-Hispanic blacks
and non-Hispanic whites. Similar to our results, two cross-sectional
studies
did not observe significant differences in
circulating SHBG concentration between young adult black and white men (17, 19), whereas a third study reported a higher SHBG concentration in young African-American than Caucasian men (6).
To date, Hispanic males infrequently have
been examined concerning their sex steroid hormone profile. In a
cross-sectional
study that included 200 Hispanic men aged 31–44 yr
old, Hispanics had a testosterone concentration that was similar to the
concentration in non-Hispanic white but lower than
in black men (9). Similarly, no differences in total testosterone concentration were observed in the Boston Area Community Health Survey,
which included 648 Hispanics, aged 30–79 yr (21). In the Hawaii-Los Angeles Multiethnic Cohort (8),
which included 523 U.S. Latinos, aged 47–74 yr, U.S. Latinos had a
slight but not significantly lower circulating testosterone
concentration than U.S. whites after adjusting for
age. AAG concentration was higher than the concentration in
African-American
men and lower than in U.S. whites, but neither
difference was statistically significant (8).
In NHANES III, we studied Mexican-American men, which is the largest
Hispanic group in the United States. Whether our results
for Mexican-American men may be compared with the
results in other Hispanic populations may depend on the composition of
those
Hispanic populations by country of origin.
Several aspects of our study merit
further discussion. First, sex steroid hormone and SHBG concentrations
in humans are influenced
by a number of factors. Our goal was to determine
whether there was racial variation in hormones beyond the variation due
to differences in prevalence of modifiable factors
that influence hormone concentrations. Therefore, we adjusted the
regression
models for factors that correlate with hormones and
that differ by race, i.e. percent body fat, cigarette smoking,
alcohol consumption, and physical activity. However, it should be noted
that these
modifiable predictors of hormone concentrations are
also risk factors for chronic diseases and that hormones may mediate
their
influence on disease risk. Thus, assessment of
crude (or age-adjusted) differences in hormone concentrations is key to
understanding
the contributions of hormones to the racial/ethnic
variation in the burden of disease. Second, serum testosterone
concentration
exhibits diurnal variation. In one study, mean
testosterone concentrations were 25–30% lower at 2000 h than at 0800 h,
which
was similar in African-American and Caucasian men (6).
Therefore, we selected only men who participated in the morning session
of the first phase of NHANES III (0830–1130 h).
Additionally adjusting for time when blood was
drawn did not appreciably change the results. Third, due to the number
of comparisons
we evaluated, we cannot exclude chance as an
alternative explanation for any given finding. Fourth, NHANES III is a
cross-sectional
study representative of the civilian
non-institutionalized U.S. population, thus aiding in the broad
generalizability of these
results. Main characteristics, such as age, percent
body fat, smoking, alcohol consumption, or physical activity, of the
subset
of men used in this analysis were comparable to all
men 20 yr and older who participated in the morning session of the
first
phase of NHANES III (data not shown). Also, the
over-sampling of minorities and elderly and the large sample size
allowed
for reasonably stable estimates even after
adjusting for possibly confounding variables. Fifth, the analyses were
based on
a single hormone measurement and may not perfectly
reflect serum hormone levels averaged over time (39), although some studies have shown that using only one sample was highly accurate in predicting sex steroid hormone levels
for a time frame up to 3 yr (26, 40). Sixth, NHANES III is a cross-sectional study, and thus, we could not assess differences in the hormones trajectories over
age by race/ethnicity.
In conclusion, in this large, nationally
representative sample, there was no difference in circulating
testosterone concentrations
between non-Hispanic black and white men overall.
However, black men had the highest estradiol level overall across all
ages,
which was not explained by racial differences in
the prevalence of factors that influence hormone levels.
Mexican-American
men had hormonal profiles similar to non-Hispanic
white men, with the exception of higher testosterone. Given these
findings,
it may be equally if not more important to
investigate levels of estradiol than testosterone in relation to
diseases that
show racial disparity, such as prostate cancer.
Footnotes
-
This study is the first from the Hormone Demonstration Program, which is supported by the Maryland Cigarette Restitution Fund Research Grant Program at the Johns Hopkins Medical Institutions. S.R. was supported by the Fund for Research and Progress in Urology, James Buchanan Brady Urological Institute, Johns Hopkins Medical Institutions.
-
Disclosure: The authors have nothing to disclose.
-
First Published Online April 24, 2007
-
Abbreviations: AAG, Androstanediol glucuronide; BMI, body mass index.
- Received January 5, 2007.
- Accepted April 16, 2007.
Strange !
ReplyDeleteVermeulen A could do miracles.
Survey questionnaire analysis