Effects of dietary fat and fiber on plasma and urine androgens and estrogens in men: a controlled feeding Joanne Beverly Philip
F Dorgan, Joseph T Judd, Christopher Longcope, A Clevidence, William S Campbell, Padmanabhan R Taylor
ABSTRACT We conducted a controlled evaluate the effects of fat and fiber consumption urine
sex hormones
domly diet
in men.
43 healthy assigned
men
to either
other
diet.
The body
both
diets.
with
a ratio
whereas
a 2-wk
energy
but
low-fat
of
was 13.3
18.8%
to
provided
kcal)/d
of energy fat
from
(P:S)
of energy
of
from
on the high-fat,
low-fiber
high-fiber
was
low-fat,
fraction also
(P
was
0.04).
=
Men’s
13% higher
low-fat,
12-28%
Results
lower
of this
hormone
and with
study
estrone
in
their
the high-fat,
suggest
metabolism
that
diet
Conversely,
and diet
may
Am
than
urinary
(P
0.01).
endogenous
Cliii
Nutr
fat
hormone
sex
Diet,
dietary
fats,
dietary
fiber,
on
serum
the
low-fat,
fat
(10,
than
studies
(12-14).
reported
in men
include
correlated
in
three
diet
dietcorrela-
vegetarian
Agriculture
feeding
study
fat
and
cancer
(21),
fiber
or
studies but
with
and Beltsville
prostaglandins
on
Human con-
the effect
several
indexes
including
(22),
fecal
we evaluated urine
for
Service,
to evaluate
and
(18-
findings
atherosclerosis,
on plasma
and
components inconsistent
Research intakes
fiber
depressed
diet,
in men
As part of this study, components
with
vegetarians
were
inconsistent. Cancer Institute
to
estradiol
intervention levels
Center,
lipoproteins
hormone
positive
of specific dietary studies have been
or
dietary
sex
Specific
between
testosterone
related
Male testos-
(1 2), and
with
and
comparisons
a controlled
a
risk
with polyunsaturated fat (13) and divegetable fat consumption (14) and
of testosterone
Research
1 1).
plasma
omnivores
several
with
been
and
cancer
lower
in
high-fiber
dietary
hormones
have
or urine
Nutrition
cancer
to have
concentrations
Moreover,
20),
and hormones.
androgens
sex
omnivores and correlations with hormones from different
these
to animal
prostate
fiber
correlations
ducted
due
modifies
reported
(1 2). However,
potentially
estrogen,
diet
the
been
tions of testosterone hydrotestosterone
plasma WORDS
and
of modifying
l996;64:
850-5. KEY
effect
relations
inverse
primarily
a hormone-dependent
other hormones were In 1986 the National
metabolites
diet
alter
J
the
is
and estradiol
intake
was
is that
have
(12-17).
with
their
2-hydroxy
low-fiber
men.
from
of testosterone
low-fiber
an
vegetarians
fat
SHBG-bound
excretion
0.01).
=
for the
urinary
the high-fat,
(P
diet
of estradiol
diet and the difference
significant
daily
with
high-fiber
excretion were
diet
cancer
concentrations
fat with
association
hypothesis
dietary
-
the
Prostate current
terone
1.3,
the
and
(8).
on
a P:S of 0.6. Total dietary fiber consumption from the low- and high-fat diets averaged 4.6 and 2.0 g MJ ‘ - d ‘, respectively. Mean plasma concentrations of total and sex-hormone-bindingglobulin (SHBG)-bound testosterone were 13% and 15% higher, respectively,
and
consumption
through
to the
to maintain
(3170
saturated
41.0%
over
varied
MJ
ran-
low-fiber
crossed
intake,
and
initially
or high-fat,
of diets
diet provided
design
were
period
averaged
diet
a crossover
y. Men
high-fiber
polyunsaturated
the high-fat
had
washout
content
weight
The
study 19-56
a low-fat,
for 10 wk and after
constant
The aged
feeding study to on plasma and
Brown, Arthur Schatzkin, Charlene Franz, Lisa Kahie,
mutagens,
the effect androgens
of and
estrogens.
INTRODUCTION
1
From
the
Division
of Cancer
Prevention
and
Control,
National
Diet, particularly fat consumption, has been implicated as a risk factor for prostate cancer. Prostate cancer mortality is
Cancer Institute, Bethesda, MD; the Diet and Human Performance Laboratory, Beltsville Human Nutrition Research Center, ARS, US Department of Agriculture, Beltsville, MD; the Departments of Obstet-
higher
fat
rics
and
an
ical
School,
in countries
is elevated increased
(1), risk
where and of
per capita
high-fat
diets
prostate
consumption have
cancer
been
of animal associated
in several
with
and
case-control
studies
Study,
a prospective
advanced those 850
(2-9).
prostate in the
highest
In
the
study cancer
Health
of 51 529 was
compared
1.79 with
Professionals men,
the
(95%
CI
the
lowest
Follow-up relative
risk
for
1.04,
3.07)
for
=
quintile Am
J Clin
of fat Nutr
and
Worcester,
Spring,
MD.
Address
reprint
requests
Institute, Bethesda,
Executive Plaza MD 20892-7326.
Received
February
Accepted
for publication
1996;64:850-5.
Printed
Medicine, MA;
Inc, Silver 2
cohort
Gynecology
15,
in USA.
and
University Information
to IF Dorgan,
of Massachusetts
Mcd-
Management
CPSA,
DCPC,
Services,
National
North, Room 211, 6130 Executive E-mail:
[email protected].
Cancer
Boulevard,
1996.
July 25, 1996. © 1996 American
Society
for Clinical
Nutrition
Downloaded from www.ajcn.org by guest on July 15, 2011
included
Charles P Nair,
DIET SUBJECTS
AND
ENDOGENOUS
SEX
Testosterone,
METHODS
AND
HORMONES dihydrotestosterone,
in plasma Healthy male volunteers aged 19-56 y from the Beltsville, MD, area who met the following criteria were recruited for the controlled feeding study in 1986: 1) no history of diabetes, cancer,
or cardiovascular,
disease;
2) no medication
sic;
kidney,
3) a weight-for-height
based
on
normal
1983
results
Metropolitan from
or chronic
Life
a physical
Insurance
was
approved
tables
examination,
(23);
4)
a com-
and 5) no adherence research with human
by the Institutional
Review
Boards
design.
Participants
were
paired
age,
smoking status, and body mass index, and one man from each pair was randomly assigned to each diet. After 10 wk on the diet and a 2-wk washout period, participants were crossed over to the other diet for 10 wk. All meals were prepared in the Human Study Facility at the Beltsville
Human
subjects
ate
Nutrition
breakfast
and
Research dinner
Center. in the
On
dining
weekdays
room
at this
facility and lunches were provided at breakfast for consumption later in the day at work or at home. On weekends subjects ate prepackaged meals at home. No foods other than those provided
by
Sweeteners to those recorded
the
study
were
permitted
except
tea
and
coffee.
and other additives to these beverages were limited provided by the study, and quantities used were by participants. Salt was allowed ad libitum and
consumption
was
estimated
by using
tared
salt
shakers.
Water
of known mineral content was provided to participants. Alcohol and vitamin and mineral supplements were prohibited. Men were weighed on each weekday and the energy content of the diets was varied in l.7-MJ (400-kcal) increments to maintain constant body weight. Diets provided all known nutrients (24).
in amounts Nutrient
to
meet
composition
recommended was
calculated
celite
Horton
(DHEAS)
measured
was
Group
Ltd,
bound
and
an
Urinary
-glucuronidase.
urinary
sephadex
males
analyte,
plasma
analyzed
variability hormone
control
samples
averaged
11.8%
for
same
8.2%
CV
for
glucuronides
for
estradiob,
20.8%
samples
the
catechols,
the
droxyestrone Because not normal,
CV
Methods
proposed and
period
by
diet
Fleiss
effects.
1 to period
(36) To
were
determine
of
free
all
1 with
(SHBG,
the
=
0 when
testosterone; DHEAS,
vegetarian
Serum
0.1
42.7
-
-6.1,
2.3
0.12
10.3, 4.4
0.46
30.7,
55.7, 72.2
64.9
56.5, 74.1
removal
of outliers:
total
using
all observations
estradiol
dihydrotestosterone;
androstanediol
and
1.7
-2.9
1), free estradiol
(n
glucuronide,
based
diet
compared
with
“0.5
estrone,
with
sex
hormones
were
measured
after
on a
SHBG-bound and
(n
-
I), albumin-bound
0.31 0.15
estradiol
(n
3).
total,
test when
t
differences
estradiol)
and
free,
albumin-bound
and
were
a Wilcoxon
normally
rank-sum
test
distributed when
(total,
free, not
differences
were
estradiol).
provided 25% of energy as fat with a P:S of 1.22. After the intervention, men had significantly lower serum concentrations of androstenedione and total and free testosterone. However,
the
concentrations
of dihydrotestosterone,
DHEAS,
estradiol,
and
estrone did not differ between the two periods. Reed (39) failed to detect a difference in total testosterone in six men following isoenergetic diets providing 20 and 100 g fat/cl. Because SHBG concentrations increased, however, free testosterone decreased after the low-fat diet. Our finding of greater daily urine testosterone excretion in men consuming a high-fat, low-fiber diet relative to men consuming a low-fat, high-fiber diet is consistent with the findings of most controlled feeding studies. We also observed elevated plasma testosterone concentrations when men ate the high-fat, low-fiber diet, but the difference from concentrations in men who consumed the low-fat, high-fiber diet was significant only
a 2-wk
period when men consumed their usual diets, which provided 40% of energy as fat with a P:S of 0.15 and again after a 6-wk intervention period when men consumed isoenergetic diets that TABLE
-0.6,
36.3
content of the vegetarian diet was of the meat diet. Predict serum concentrations of testosterone were comparable and decreased significantly by 35% after the vegetarian diet but not after the meat diet. Differences in other androgens and estrogens were also reported, but these were attributed to dissimilarities in baseline concentrations. Hamabainen et al (19) studied the effect of modifying dietary fat on serum sex hormones in 30 healthy, free-living men old.
-18.7,5.0
-0.3
37.4
meat diet and the fiber approximately twice that
40-49-y
-6.8
2.1,
each for 6 wk. The diets were isoenergetic and “‘28% of energy was derived from fat on both diets. The P:S, however, was
120.3 2.8
2.4
sulfate.
for test of H0: difference
albumin-bound,
after
2.5
3 mean
Geometric
(95%
CI) amounts
and mean High-fat
(95% CI) differences ,
low-fiber
Mean
in daily
diet
urine
Low-fat,
95% Cl
hormones
by diet
high-fiber
Mean
diet
High- fat diet
95% CI
Difference’
-
low-fat
95%
CI
9.6,
42.6
diet P
Glucuronides Testosterone
Estrone
(nmol/d)
207.4
(nmolld)
3.8
3.4, 4.3
6.8
5.5,
(nmol/d)
Catechols 2-hydroxyestrone (nmol/d) 2-hydroxyestradiol (nmolld) I Mean differences of untransformed 2
124.6,
1 1.1
Estradiol Estriol
161.3
(nmol/d)
p value
2-hydroxyestrone,
for
test
of
H0:
71.8 9.3 values
difference
2-hydroxyestradiol)
=
and
143.0
9.8, 12.6 8.3
65.1, 78.6 8.1, 10.7 after removal of outliers:
0 when a Wilcoxon
using
test
when
180.8
26.1
12.3, 15.6
-2.4
-3.4,
4.3
3.7, 4.9
-0.6
-
6.8
5.5,
85.2 12.9 testosterone
all observations
rank-sum
1 12.5,
13.8
based differences
8.4
76.4, 94.1 1 1.5, 14.4 (n
=
on a
I
were
-
(n
test when
differences
not
normally
0.0002 0.008
0.3
-0.7,
1.4
0.57
14.6 -3.4
-21.6, -4.8, 1).
-7.5 -2.0
0.0003
