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Nutrition and Cancer
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Food Sources of Phytoestrogens and Breast Cancer Risk
in Mexican Women
Luisa Torres-Sànchez , Lizbeth López--Carrillo , Malaquías Ló--Cervantes , Celina Rueda-
Neria & Mary S. Wolff
Published online: 18 Nov 2009.
To cite this article: Luisa Torres-Sànchez , Lizbeth López--Carrillo , Malaquías Ló--Cervantes , Celina Rueda-Neria & Mary S.
Wolff (2000) Food Sources of Phytoestrogens and Breast Cancer Risk in Mexican Women, Nutrition and Cancer, 37:2, 134-139,
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NUTRITION AND CANCER, 37(2), 134–139
Copyright © 2000, Lawrence Erlbaum Associates, Inc.
Food Sources of Phytoestrogens and Breast
Cancer Risk in Mexican Women
Luisa Torres-Sánchez, Lizbeth López-Carrillo, Malaquías López-Cervantes,
Celina Rueda-Neria, and Mary S. Wolff
Abstract: We analyzed the intake of selected foods that con-
tain phytoestrogens in relation to breast cancer (BC) risk
using data from a hospital-based case-control study per-
formed in Mexico City from 1994 to 1995. A total of 198
women with BC, aged 21–79 years, were individually age
matched to an identical number of women with no breast
disease. By a direct interview, information on socioeco-
nomic characteristics and diet was obtained. A semiquanti-
tative questionnaire was used to estimate the frequency of
consumption of 95 foods. The effect of selected foods that
contain phytoestrogens on BC risk was estimated using lo-
gistic regression models. The adjusted odds ratio for the
consumption of more than one slice of onion per day and BC
was 0.27 (95% confidence interval = 0.16–0.47), with a sta-
tistically significant trend (p < 0.001). This protective effect
remained after adjustment for known risk factors of BC.
Among premenopausal women, there was also a protective
and significant effect due to the intake of lettuce and spinach
and nonsignificant protective effects for the consumption of
apples and herbal tea. Additional studies aimed at evaluat-
ing the potential protective effect of particular phytoestro-
gens on BC risk are needed.
Urinary levels of the lignans equol and enterolactone were
associated with a substantial reduction of BC risk in an epi-
demiological study performed in Australia (17), and a simi-
lar reduction in BC risk was also the case with the urinary
levels of total isoflavonoids in a recent study performed in
Shanghai (18).
BC mortality is higher in the United States than in Japan
(32.7 vs. 11.3 per 100,000) and also much higher than in
Mexico (7.1 per 100,000) (19). The consumption of foods
rich in phytoestrogens, which are common in the Mexican
diet (20) (e.g., onion, lettuce), might play a protective role in
the BC incidence.
We evaluated the intake of foods that contain phyto-
estrogens in relation to BC risk in women from Mexico City.
Material and Methods
From March 1994 to August 1995 a hospital-based case-
control study was carried out in Mexico City. The study popu-
lation was assembled from women seeking care at three large
public hospitals of Mexico City (Instituto Nacional de Can-
cerología, Hospital General, and Hospital Gea González).
A total of 198 recruited cases were women between 21
and 79 years of age. Participants had a histologically con-
firmed diagnosis of BC, were being seen for the first time at
the participating hospitals with no previous treatment for
BC, were free from any other type of cancer, and had lived
in the Mexico City Metropolitan Area for ³20 years. Tumor
stage was classified using the tumor, nodes, metastasis
(TNM) system.
For each case we selected one age-matched control ( 3
yr) from other clinical services of the participating hospitals,
except gynecology and oncology. These controls had no his-
tory of cancer or any other breast disease, and they had lived
in the Mexico City Metropolitan Area for ³20 years.
Dietary, reproductive, and socioeconomic information of
the study population was obtained by means of a personal
Introduction
It has been suggested that phytoestrogens, which are
hormonelike compounds found in plant foods, might play a
protective role in the etiology of breast cancer (BC) (1–3).
Evidence from epidemiological studies suggests that the in-
take of some fruits and vegetables (4), such as soy (5–9),
might reduce the risk for BC. Isoflavones are found in soy
products (10), whereas other vegetables and fruits contain
lignans and flavonoids, respectively (11,12).
Flavonoids and lignans are phytoestrogens that inhibit
some types of tumor growth in vitro (13) and weakly bind to
estrogen receptors (14,15), hence, becoming potentially
anticarcinogenic compounds. The consumption of soy milk
decreased serum estrogen levels in a Japanese study (16).
L. Torres-Sánchez, L. López-Carrillo, M. López-Cervantes, and C. Rueda-Neria are affiliated with the Center for Research on Health Services, National
Institute of Public Health, Mexico, CP 62508, Cuernavaca, Morelos, Mexico. L. López-Carrillo is also affiliated with the Center for Research and Advanced
Studies, National Polytechnic Institute, CP 07300, Mexico City, Mexico. M. S. Wolff is affiliated with the Division of Environmental and Occupational
Medicine, Department of Community Medicine, Mount Sinai School of Medicine, New York, NY 10029-6574.

structured interview. Every woman was measured and weighed
to estimate the body mass index (Quetelet index, kg/m2).
A modified version of a previously validated semiquanti-
tative food frequency questionnaire that showed good repro-
ducibility, including 95 food items, was used for the study
(21). Cases were queried about their dietary habits during
the 12 months before onset of symptoms. Controls were que-
ried about their dietary habits during the 12 months before
the interview. The daily frequency of consumption accord-
ing to a predetermined portion size was obtained for each
food item. Response options ranged from never to six times
per day. The consumption of vegetables and fruits was cor-
rected for seasonal availability.
birth, or nulliparous), lifetime lactation history (accumulated
months of breast-feeding), family history of BC (yes/no),
and Quetelet index (kg/m2).
Trends across levels of food consumption were tested by
using daily frequency of consumption for foods with two
categories of consumption or by fitting the categorical vari-
ables as continuous for foods with more than two categories
of consumption. All these analyses were performed using
Stata software (24).
Results
For the present analysis, we selected individual food
items that are frequently consumed in Mexico and have been
reported to be sources of phytoestrogens, namely, onion, tea,
apple, lettuce, and spinach (12,22,23).
Odds ratios (OR) for the total study population and by
menopausal status were estimated by means of logistic re-
gression models and adjusted for age, total energy intake
(kcal), number of children, and age at first birth (³3 children
and <20 yr at 1st birth, <3 children and <20 yr at 1st birth, ³3
children and ³20 yr at 1st birth, <3 children and ³20 yr at 1st
On average, participating women were 49 years old
(range 21–79 yr). Their reproductive characteristics in rela-
tion to BC risk are shown in Table 1. The risks for BC were
higher among nulliparous women, those with fewer than
four births, those with older age at first birth, and those with
positive familial BC history. In contrast, breast-feeding after
the first delivery and all deliveries was protective. Age at
menarche, menopausal status, and obesity (measured by
Quetelet index) did not show significant associations with
BC risk in this study population.
Table 1. Age-Adjusted ORs for Known Breast Cancer Determinant Factors in the Study Populationa
P Value
Variables
OR
95% CI
for Trend
Age at menarche
³12 yr
1.0
<12 yr
0.89
0.51–1.54
Parity
³4
1.0
>1–3
2.31
2.85
1.46–3.67
1.52–5.37
Nulliparous
Age at 1st birth
<20 yr
0.000
0.002
1.0
>20–24 yr
³25 yr
Breast-feeding at 1st birthb
>0 mo
2.12
3.00
1.16–3.84
1.47–6.15
1.0
>1–6 mo
>7–12 mo
>12 mo
Breast-feeding all birthsb
>0 mo
0.89
0.76
0.60
0.45–1.75
0.39–1.52
0.27–1.35
0.20
1.0
>1–6 mo
>7–12 mo
>12 mo
1.17
0.58
0.50
0.44–3.06
0.22–1.58
0.22–1.15
0.020
Menopausal status
No
1.0
Yes
1.18
0.62–2.24
1.29–6.43
Familial breast cancer
No
Yes
1.0
2.88
Quetelet index
£24 kg/m2
>25–29 kg/m2
³30 kg/m2
1.0
0.84
1.05
0.52–1.35
0.60–1.84
0.89
a: Abbreviations are as follows: OR, odds ratio; CI, confidence interval.
b: Nulliparous women were excluded.
Vol. 37, No. 2
135

Table 2. Effect of Intake of Some Selected Foods on Breast Cancer Risk
Adjusted ORa
(95% CI)
Foods
Cases
Controls
Vegetables
Leafy green-yellow,b portions/wk
<2.5
2.5–4.0
>4.0
82
48
51
63
62
65
1.00
0.76 (0.43–1.36)
0.56 (0.30–1.07)
Nonleafy yellow-orange,c portions/wk
<1.5
1.5–4.0
>4.0
74
52
61
61
68
65
1.00
0.58 (0.31–1.08)
0.79 (0.41–1.52)
Fruits
Citrus,d,f portions/wk
<5.0
5.0–11
>11
Noncitrus,e portions/wk
83
45
62
65
65
65
1.00
0.43 (0.23–0.81)
0.44 (0.20–0.98)
<3.5
3.5–8.0
>8.0
69
58
61
61
69
64
1.00
0.55 (0.28–1.07)
0.80 (0.36–1.83)
Fish, portions/wk
Never
<1
1–1.5
>1.5
27
53
65
53
20
55
62
61
1.00
0.72 (0.29–1.79)
0.89 (0.34–2.30)
0.67 (0.26–1.72)
Meat (beef), portions/wk
<1
³1
64
127
70
126
1.00
1.34 (0.77–2.31)
a: Adjusted by total energy intake (kcal), age at menarche (yr), number of children and age at 1st birth (³3 children and <20 yr at 1st birth, <3 children and
<20 yr at 1st birth, ³3 children and ³20 yr at 1st birth, <3 children and ³20 yr at 1st birth, nulliparous), lifetime lactation (mo of breast-feeding), family his-
tory of breast cancer (yes/no), menopausal status (pre/post), and Quetelet index (kg/m2). Values in parentheses are 95% CIs.
b: Includes lettuce, spinach, cauliflower, and squash flower.
c: Includes beets, carrots, and zucchini.
d: Includes orange, tangerine, pineapple, and strawberries.
e: Includes banana, plums, peach, apple, grapes, pear, papaya, mango, watermelon, cantaloupe, and local fruits (marney, tuna, and zapote).
f: t-Test for trend, p < 0.05.
The effects of selected food items on BC risk are presented
in Table 2; nonsignificant protective effects were observed
for the consumption of particular groups of vegetables (leafy
green-yellow and nonleafy yellow-orange) and citrus fruits
and for all categories of fish intake. In contrast, meat (beef)
intake showed a nonsignificant increased risk.
this disease is a recent finding. One other recent case-control
study from France investigated the role of diet in BC and re-
ported a reduction of 60–75% in BC with high consumption
of onion and garlic (25). Also, our results suggest that the
consumption of lettuce, spinach, herbal tea, and apples may
protect against premenopausal BC.
The adjusted OR for the consumption of foods that are
sources of phytoestrogens are shown in Table 3. Onion con-
sumption above the median was strongly protective among
premenopausal and postmenopausal women (OR = 0.27,
95% confidence interval = 0.16–0.47). In addition, among
premenopausal women, there was a significant protective ef-
fect for higher intake of lettuce and spinach. Apple and
herbal tea showed a nonsignificant protective effect on BC
among premenopausal women. Milk intake was not associ-
ated with BC risk.
These foods are also rich in the flavonoid quercetin. On-
ions are one of the richest sources of the flavonoid quercetin
(26) in the diet (10–44 mg/100 g) (22,23). Daily human in-
take of quercetin is ~16 mg/day, and it is the highest food an-
tioxidant source in the Western diet (22). Quercetin inhibits
the proliferation of human BC cells in vitro and delays mam-
mary tumorigenesis (27) in vivo. Potential mechanisms for
the anticarcinogenic effects of quercetin might include its
capacity to bind with type II estrogen receptors (28) and its
potent antioxidant activity (22).
To the best of our knowledge, this is the first epidemio-
logical study that has specifically assessed the intake of
quercetin-containing foods with respect to BC risk. The epi-
demiological evidence for the protective effect on BC due to
the consumption of vegetables, and particularly green vege-
tables, is ample and consistent, but only a few studies fo-
Discussion
Our results show that premenopausal BC risk is inversely
related to the intake of onion, lettuce, and spinach. The role
of onion intake alone as a protective agent in the etiology of
136
Nutrition and Cancer 2000

Table 3. Effect of Food Phytoestrogen Sources on Breast Cancer Risk According to Menopausal Status
Premenopausal
Postmenopausal
All
Crude ORa,b
(95% CI)
Adjusted ORa,c
(95% CI)
Crude ORa,b
(95% CI)
Adjusted ORa,c
(95% CI)
Adjusted ORa,c
(95% CI)
Foods
Cases
Controls
Cases
Controls
Onion, slice/day
<1
³1
33
53
10
81
1.0
1.0
39
66
20
84
1.0
1.0
1.0
0.20 (0.09–0.43)
0.18 (0.07–0.42)
0.004
0.38 (0.20–0.72)
0.37 (0.18–0.76)
0.01
0.27 (0.16–0.47)
0.000
t-Test for trend
Lettuce
<1 leaf/wk
³1 leaf/wk
t-Test for trend
62
24
56
35
1.0
1.0
74
31
69
35
1.0
1.0
1.0
0.59 (0.31–1.12)
0.66 (0.31–1.38)
0.04
0.81 (0.45–1.46)
0.73 (0.37–1.45)
0.30
0.70 (0.42–1.15)
0.03
Spinach
<0.5 cup/wk
³0.5 cup/wk
t-Test for trend
68
18
62
28
1.0
1.0
73
32
77
26
1.0
1.0
1.0
0.53 (0.26–1.08)
0.44 (0.20–0.98)
0.04
1.30 (0.70–2.38)
1.39 (0.69–2.78)
0.91
0.85 (0.51–1.40)
0.19
Apple
<1 piece/wk
³1 piece/wk
t-Test for trend
Herbal tea
58
26
50
40
1.0
1.0
61
44
63
41
1.0
1.0
1.0
0.54 (0.28–1.00)
0.57 (0.28–1.15)
0.25
1.10 (0.63–1.91)
0.97 (0.51–1.84)
0.64
0.83 (0.54–1.28)
0.84
Never
28
31
26
17
47
27
1.0
1.0
26
49
28
24
51
29
1.0
1.0
1.0
<3 cups/wk
³3 cups/wk
t-Test for trend
0.41 (0.20–0.87)
0.59 (0.26–1.32)
0.41 (0.18–0.92)
0.68 (0.28–1.62)
0.45
1.14 (0.58–2.27)
1.12 (0.52–2.40)
1.32 (0.62–2.82)
1.54 (0.67–3.54)
0.31
0.75 (0.44–1.30)
1.04 (0.57–1.88)
0.83
a: Values in parentheses are 95% CIs.
b: Adjusted by age.
c: Adjusted by total energy intake (kcal), age at menarche (yr), number of children and age at 1st birth (³3 children and <20 yr at 1st birth, <3 children and <20 yr at 1st birth, ³3 children and ³20 yr at 1st birth, <3
children and ³20 yr at 1st birth, nulliparous), lifetime lactation (mo of breast-feeding), family history of breast cancer (yes/no), Quetelet index (kg/m2).

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Acknowledgments and Notes
The authors thank Reina Collado for typing the paper. This study was
partially supported by grants from the Secretary of Health of Mexico, the
John D. and Catherine T. MacArthur Foundation, the National Cancer In-
stitute, and Fogarty International Center of the National Institutes of
Health Grant D43 TW00640 to the Mount Sinai/Queens College Interna-
tional Training Program in Environmental and Occupational Health. This
work was done in three large public hospitals of Mexico City (Instituto
Nacional de Cancerología, Hospital General, and Hospital Gea González).
Address correspondence to Lizbeth López-Carrillo, Ph.D., National Insti-
tute of Public Health, Av. Universidad No. 655, Col. Sta. María
Ahuacatitlán, CP 62508, Cuernavaca, Morelos, México. Phone: (73) 11-
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Submitted 22 July 1999; accepted in final form 13 March 2000.
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