The relationship concentrations postmenopausal Joilo

C Barbosa,

Terry

among adiposity, diet, and hormone in vegetarian and nonvegetarian women13 D Shultz,

Shelby

J Filley,

and David

ABSTRACT The relationships among anthropometric variables, dietary nutrients, and plasma steroid, polypeptide, and binding-protein hormone concentrations were investigated in 24 Seventh-day Adventist postmenopausal women, 12 vegetarian (SV) and 12 nonvegetarian (SNV). Fasting blood and 7-d dietary intake information were collected. SVs consumed significantly more crude and dietary fiber and fewer saturated fatty acids than did SNVs. The thigh and sum of three skinfold-thickness measurements were significantly greater for SNVs than for SVs. Plasma concentrations of estradiol-l7 were significantly lower in SVs than in SNVs. Significant relationships were observed for the combined groups (SV and SNV) between estradiol-l7fl and triceps and suprailiac skinfold thicknesses and body fat. Plasma concentrations of estradioll7fl ofthe combined groups revealed a significant negative relationship between their crude and dietary fiber intakes. Further study delineating the effects of adiposity and dietary nutrients on basal concentrations ofsex hormones is warranted. Am JClin Nutr l990;5l:798-803. KEY WORDS Seventh-day Adventist, diet-hormone relationships, skinfold, adiposity, estradiol-l 7, breast cancer

anthropometryleanness, fiber,

C Nieman excretion of endogenous estrogens. Goldin et al (1 1) reported lower plasma and urinary estrogen concentrations in premenopausal vegetarian women than in nonvegetarians. Goldin et al (1 1) surveyed vegetarian women who had diets lower in fat (30% of calories) and higher in dietary fiber (28 g/d) than the average American omnivorous diet but the proportion of fat was not at the remarkably lower level (20% calories as fat) seen among Asian women ( 13), who have the lowest breast-cancermortality rates in the world. In an effort to address this issue, Goldin et al (1 3) found that Asian premenopausal and postmenopausal

women

possibly

because

12,

14,

Seventh-day

Adventist

(SDA)

women

experience

lower

mor-

from breast cancer than does the general California population (1-3). It has been suggested that this may be due to their dietary habits because 50% are lactoovovegetarians (1-3). Mills et al (3) recently found no significant relationship between the consumption of animal products (ie, meat, milk, cheese, and eggs) and breast-cancer mortality among SDAs. The possible association between dietary fiber and risk of breast cancer was not determined. Epidemiologic studies have demonstrated associations between dietary nutrients, especially fat and fiber, and the mcidence of hormone-dependent cancers, including breast cancer (4-6). Recent studies indicate that diet may modify sex-hormone metabolism in both men and women (7-16). Indeed, women consuming various diets-vegetarian or nonvegetarian and low- or high-fat-had different plasma, urine, and fecal concentrations ofestrogens (9-16). Diet appears to influence the production, metabolism, and 798

Am

J C/in

Nuir

1990;5l:798-803.

Downloaded from https://academic.oup.com/ajcn/article-abstract/51/5/798/4695325 by Denise Hannibal user on 12 April 2018

of adipose

1 5) studies

reduce

tabolism.

tality

ate low-fat

(20%

ofcalories)

diets

had

tissue

loss.

This

suggests

that

the

influence of a low-fat diet may not have been fully considered because adipose tissue is the major source of estrogen formation in postmenopausal women (I 7). These as well as other (9, may

Introduction

who

lower plasma estrogen concentrations than did American omnivorous women. In another study Boyar et al ( 16) found that serum concentrations of estradiol17$ but not of estrone were significantly reduced in postmenopausal breast-cancer patients placed on a low-fat diet (20% of calories) for 5-6 mo. Mean body weight decreased by ‘-2.3 kg during the same time (16),

suggest

that

a low-fat

and/or

high-fiber

diet

breast-cancer Further

risk through effects on estrogen meresearch is needed to define more precisely among adiposity, dietary nutrients, and estro-

the relationships gen metabolism. The objective of this study was to characterize those dietary and hormonal variables that may explain the observations of lower mortality from breast cancer among SDAs. Herein we describe the hormonal status and interrelation ofdietary nutrients with plasma steroid and polypeptide hormone profiles of postmenopausal SDA women habitually following vegetarian (SV) and nonvegetarian (SNV) dietary regimes. In addition, relationships between various anthropometric variables and plasma I

hormone

From

concentrations

the Department

the Departments

of Health

are

of Biochemistry, Science

reported.

School

and Nutrition,

of Medicine, School

and

of Public

Health, Loma Linda University, Loma Linda, CA. 2 Supported in part by a grant from the Callicott Foundation (TDS). 3 Address reprint requests to TD Shultz, Department of Food Science and Human Nutrition, Washington State University, Pullman,

WA 99164-6376. Received April 4, 1989. Accepted for publication Printed

in USA.

June 7, 1989.

© 1990 American

Society

for Clinical

Nutrition

ADIPOSITY-DIET-HORMONE

RELATIONSHIPS

Methods Subject

selection

Elderly

female

subjects

were

initially

recruited

from

mem-

bars

of the Adventist Health Study, a prospective cohort involving 6 y (1977-1982) of follow-up of 34 198 Caucasian SDAs, including 20 341 women living in California. Participants were chosen who resided within a 160.9-km radius of the Loma Linda University campus. Women were contacted by telephone. vidually

Subjects who volunteered sent a questionnaire that

to participate requested detailed

information regarding their medical their use ofdrugs. These questionnaires the

health

of the

to potential consent

The

participants before

Loma Linda A sample from

subjects.

and

acceptance.

University’s of SV and

the volunteers.

study

dietary histories and were used to ascertain

protocol

was

each

subject

signed

The

protocol

was

The

SV group

consisted

explained

an informed

than once a month 25 y. Additional

and

had

by

Studies. was selected

of 12 women

12 women aged 64-83 if they ate meat, fish, followed

this

aged

y. Subjects or poultry dietary

regi-

selection criteria were as follows: normal weight to minimally obese [body mass index (BMI, kg! m2), 20-29.9] (1 8) and no history ofcancer, cardiovascular disease,

hypertension,

group

comprised

ject; obese

the

diabetes,

1 1 normal-weight

SNVs

comprised

subjects.

coids, treated lism.

with

Sampling

and

Subjects

individual

describing

started

or

any had

hormone

nutrient

and saturated

before

food

combinations their

diets

by telephone.

Upon

included.

analysis

(19)

carbohydrate,

fatty acids,

Foods

they

and

oleic and linoleic

as cassewere

given

completion,

each

to ensure

that

coded

for corn-

were

of 10 dietary crude

writ-

estimat-

(such after

by the nutritionist

was

with

intake,

variables:

dietary

all food

fiber,

total

fatty acids,

and cho-

obtained

from

lesterol.

Blood antecubital

collection. vein

Blood ofeach

samples

subject;

samples were drawn into 0700 and 0900. Aliquots

after

heparinized ofplasma

were

an overnight

evacuated were stored

analyzed. Samples assays were frozen

for sex-hormone-binding at -70 #{176}C until assayed.

the morning

the

after

7-d diet

record

fast,

the

20-mL

tubes between at -20 #{176}C until

globulin (SHBG) All blood was drawn

was completed.

Anthropometric measurements. Weight (wt) and height (ht) were determined by the use of a calibrated physician’s scale and a wall-mounted measuring tape. Shoes and outerwear were removed before weighing. BMI was calculated as an estimate of obesity (20, 2 1). The three-site skinfold test was used as a second indicator of body fat. Triceps, suprailiac, and thigh

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in duplicate

Industries,

with

Analyticalmethodologyfor and binding-protein

polypeptide,

Plasma (DHEA-S), by

steroid,

estradiol1 7/3, growth hormone,

commercially

RIA

dehydroepiandrosterone-sulfate and prolactin were determined

purchased

(RIA) kits CA). All hormones, with the sulfate, were measured by di-

radioimmunoassay

Inc, Carson, and estrone

of25-l00

ethyl

MD), regres-

hormones

(ICN Biomedicals exception ofestrone rect

Lange

Cambridge,

by use ofa quadratic

L

plasma.

Estrone

was

measured

by RIA

(3:2, vol:vol) extraction and punfication on 0.5 cm X 5 cm Sephadex LH-20 (Sigma Chemical Co, St. Louis) columns as previously described by Shultz et al (24). The mean (±SD) recovery of[3Hjestrone added to plasma was 86 ± 9%. Values were corrected for recovery ofthe tritiated internal standard. All assays were performed in duplicate; in each assay series an equal number ofsubjects from each group was included. Individual assays were monitored by quality control samples (ICN Biomedicals Inc) included in each group of unknowns. All assays were performed with the use of highly specific

acetate-hexane

antiserum

tivity.

Kits

from

Farmos

that

for

in

(Beckman

been

measured

with the percent body fat estimated sion equation (22, 23).

counters Estrone

collection

along

Scientific

type

metabo-

sample

booklet

were

(Cambridge

counted

glucocortiif they

for reporting

to record

was reviewed

protein,

weeks

procedures

information

puterized energy,

6 mo

to influence

Two

instruction

record

relevant

known

used

thicknesses

calipers

sub-

4 minimally

had

progesterone,

past

SV

obese

and

ifthey

estrogens,

The

1 minimally

a 7-d food-record

and

ing portions, roles).

excluded

the

drugs

assessment. were mailed

ten instructions

food

(ie, within

other

and

disease.

procedures

Dietary subjects

were

therapy

or thyroid)

or kidney

8 normal-weight

Women

of hormone

or liver

skinfold

after

approved

Committee on Human SNV Caucasian women

66-80 y and the SNV group, were classified as vegetarians no more men for

and

were mdipersonal

799

exhibits

negligible

immunoradioassay

of

Diagnostica Beckman

LS-7500

Instruments (model and

(Oulunsalo, Co,

1 185, Searle, estradiol-17/3

antiserum SHBG

crossreacwere

Finland).

liquid

Fullerton,

scintillation

CA)

obtained

Samples

were

counters

or Searle

Des Plaines, IL). interassay variabilities

gamma were

15%

(n = 4) and 8% (n = 3), respectively; intraassay variabilities were 1 1% (n = 10) and 12% (n = 10), respectively. DHEA-S interassay and intraassay variabilities were 8% (n = 4) and 6% (n = 10), respectively. Prolactin and growth hormone interassay variabilities were 6% (n = 5) and 3% (n = 4), respectively; intraassay variabilities were 5% (n = 10) and 13% (n = 10), respectively. SHBG between and within CVs were 4% (n = 7) and 3% (n = 10), respectively. [6,7-3H]Estrone sulfate ammonium salt (2.22 TBq/mmol) was purchased from NEN Research Products (El DuPont de Nemours,

pure.

Wilmington,

Plasma

as previously tracted

DE).

estrone

sulfate

described

(25,

to remove

The

radiolabeled

steroid

concentrations 26).

the free estrogens,

were

Initially,

1 mL

followed

was

98%

determined

plasma

was

by enzymatic

cxhy-

drolysis of the estrone sulfate with arylsulfatase. After organic extraction further separation and purification of estrone was performed on Sephadex LH-20 columns (24). Estrone was determined by RIA as described above. Estrone sulfate interassay and intraassay variabilities were 10% (n = 4) and 8% (n = 10), respectively. The recovery of added [3Hjestrone sulfate averaged 73 ± 6%. Values were corrected for recovery of the tntiated internal standard. St atistical

analyses

Statistical analyses were performed with the St atistical Packagefor the Social Sciences (27). Anthropometric variables, dietary

constituents,

were transformed Tests ofstatistical values. Correlations

and

hormone

and

SHBG

concentrations

to logarithmic (base 10) values for analysis. significance were based on logarithms of the between individual variables were exam-

BARBOSA

800 TABLE

and anthropometric characteristics Seventh-day Adventist vegetarian (SNV) women5 Variables

SV (n

Age(y)

75.5±

Ageat menarche(y) Age at first pregnancy (y) Age at menopause (y)

13.0 28.2 50.7

Weight

(kg)

57.4 159.6

Height (cm) Skinfold-thickness (mm)

Thigh Sum ofskinfold Body fat (%) mass

± ± ± ± ±

of the (SV) and

thicknesses

index

(kg/m2)

12) 1.2 0.3 2. 1 1.2 2.4 1.7

SNV

(n

71.5± 13.4 27.3 49.3 63.9 160.4

± ± ± ± ±

12)

=

1.6 0.5 2.4 1.3 3.3 2.1

2 1.6 14.8

± ±

2.5 2.0

30.8 67.2 27.8

±

4.4

± ±

7.7 1.2

27.7 ± 2.0 17.4 ± 2.3 39.9 ± 2.5t 85.0 ± 5.6 32.8 ± 1.5

22.5

±

0.8

24.7

±

0.8

different from SV, p < 0.01. different from SV, p < 0.05. from the triceps, suprailiac, and

1: Significantly § Calculated ness measurements

(g)

=

12)

47±4

SNV (n

=

1334

100

±

12)

54±4

13

16

Carbohydrate

(g) (%energy) Crude fiber(g) Dietaryfiber(g) Dietary fat

216±22 61 7 ± I

Total fatty acids (g) (%energy) (g/l000kcal) Saturated fatty acids

166±11 50 4 ± 0.4t

24±2

l3±lt

50±6

54±6

32

(g)

36

35±2

39±2

10±2

l7±3 12 ± 1 1

8± 1 12±5 7 ± 1 72 ± 18

kcal)

13±4 1 22

7 ±

18 1

±

51±SEM.

Results of the 7-d dietary

SV (n

skinfold-thick-

(22, 23).

med by linear-regression analysis (Pearson correlation coefficients). Mean differences in anthropometric measurements, dietary nutrient intakes, hormones, and hormone-binding protein were compared and tested with the unpaired Student’s t test (two-tailed). All statistical tests were considered to be significant at the p < 0.05 level.

Collection

5V and SNV groups

(%energy)

Oleicacid(g) Linoleic acid (g) Cholesterol(mg) thigh

ofthe

1425 ± 148w

Energy(kcal) Protein

(g/l000

5i±SEM. t Significantly

intake averages

Nutrients

measurements

Triceps Suprailiac

Body

=

AL

TABLE 2 Seven-day dietary

1

Demographic postmenopausal nonvegetarian

ET

nutrient intake data was conSubjects from each group

ducted through April and May 1988. were studied throughout that period.

The 12 SV subjects had been vegetarians for an average (±SEM)of54 ± 4 y, ranging from 30-74 y. This group included eight lactoovovegetanans, one lactovegetarian, and three vegans. The SNVs had eaten meat all their lives. Their average consumption of meat, fish, or poultry was three to four times per week. The SV and SNV participants did not differ significantly with respect to age, age at menarche, age at first pregnancy, age at menopause, weight, height, triceps or suprailiac skinfold thicknesses, body fat, or BMI (Table 1). The thigh skinfold thickness of the SNVs however, was significantly greater than that ofthe SVs. After combining individual skinfold-thickness measurements within groups, the SNVs had significantly higher summed skinfold thicknesses than did the SVs (p < 0.05). Significant relationships were observed for the two groups cornbined (SV and SNV) between estradiol-l7fl and triceps and suprailiac skinfold thicknesses (r = 0.40, p < 0.05; r = 0.37, p < 0.05, respectively) and percent body fat (r = 0.39, p < 0.05). For the combined groups linear-regression analysis also revealed significant negative relationships between SHBG and weight, suprailiac skinfold thickness, and BMI (r = -0.44, p < 0.025; r = -0.61, p < 0.001; r = -0.51, p < 0.005, respectively).

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t Significantly t Significantly § Significantly II Significantly

Table Dietary acids,

different

different different different

2 presents intakes

from SV, p