Long-term Dietary Cadmium Intake and Postmenopausal
Endometrial Cancer Incidence: A Population-Based
Prospective Cohort Study
Agneta A
˚
kesson, Bettina Julin, and Alicja Wolk
Institute of Environmental Medicine, Division of Nutritional Epidemiology, Karolinska Institutet, Stockholm, Sweden
Abstract
Environmental pollutants mimicking the effects of estrogen
aresuggestedtocontributetothehighincidenceofhormone-
related cancers, but supporting data are sparse. A potent
estrogen-like activity of the pollutant cadmium, mediated via
the estrogen receptor-A, has been shown in vivo . We
prospectively examined the association between cadmium
exposure and incidence of postmenopausal endometrial
cancer. The Swedish Mammography Cohort is a population-
based prospective cohort of 30,210 postmenopausal women
freeofcancerdiagnoseatbaseline(1987)andwhocompleted
a food frequency questionnaire at baseline and in 1997. We
estimatedthedietarycadmiumintakebasedonthequestion-
nairedataandthecadmiumcontentinallfoods.During16.0
years(484,274person-years)offollow-upbetweenthebaseline
and mid-2006, we ascertained 378 incident cases of endome-
trioid adenocarcinoma. The average estimated dietary cad-
miumintakewas15 Mg/day(80%fromcerealsandvegetables).
Cadmiumintakewasstatisticallysignificantlyassociatedwith
increased risk of endometrial cancer in all women; the
multivariate relative risk (RR) was 1.39 [95% confidence
interval (CI), 1.04–1.86; P
trend
= 0.019], comparing highest
tertileversuslowest.Amongnever-smokingwomenwithbody
massindex(BMI)of<27kg/m
2
,theRRwas1.86(95%CI,1.13–
3.08; P
trend
= 0.009). We observed a 2.9-fold increased risk
(95%CI,1.05–7.79)associatedwithlong-termcadmiumintake
consistently above the median at both baseline 1987 and in
1997innever-smokingwomenwithlowbioavailableestrogen
(BMI of <27 kg/m
2
and nonusers of postmenopausal
hormones). Our results support the hypothesis that cadmium
may exert estrogenic effects and thereby increase the risk of
hormone-related cancers. [Cancer Res 2008;68(15):6435–41]
Introduction
It has been suggested that environmental pollutants that mimic
the effects of estrogen contribute to the high incidence of
hormone-related cancers in Western populations (1). Although
this hypothesis has received extensive media attention, data have
hitherto been sparse in supporting such associations in humans
(2). More recently, cadmium, one of the most serious environ-
mental pollutants (1, 3), was proposed as a potent metallestrogen
(1, 4–6). Cadmium increases estrogen receptor a–mediated cell
proliferation (7) and possessed mutagenic properties (8, 9).
Although some in vitro estrogenicity assays showed no activity
(10), environmentally relevant doses of cadmium induced several
well-characterized estrogenic responses in vivo , including in-
creased uterine weight, hyperplasia, and hypertrophy of the
endometrial lining, induction of uterine progesterone receptor,
and complement C3 gene expression in animals (4). In addition,
after in utero exposure, cadmium affected mammary gland
development and early onset of puberty in female offspring—
both prototypical endocrine disruptor–like responses (4). Cadmi-
um has been widely dispersed into the environment through
industrial emission, waste incineration, and combustion of fossil
fuels. Even in industrially nonpolluted areas, farm land may
become contaminated by airborne deposition and by use of
cadmium-containing fertilizers and sewage sludge. A high
accumulation in agricultural crops results in the fact that plant
foods contribute to >80% of the total cadmium intake, with
bread, cereals, potatoes, roots, and vegetables being the major
sources (11).
Endometrial cancer is the cancer most suited for exploring
potential estrogenic effects of cadmium. Estrogen unopposed by
progesterone or synthetic progestins is the main factor influencing
the risk of this cancer (12).
We examined prospectively whether the estrogenic properties of
cadmium could be confirmed by a direct association between food-
cadmium and increased risk of endometrial cancer in the large
population-based Swedish Mammography Cohort.
Subjects and Methods
Study population. The Swedish Mammography Cohort was established
between 1987 and 1990, when all women who were born between 1914 and
1948 and residing in two counties in Central Sweden received a mailed
questionnaire concerning diet, weight, height, education, and parity; 66,651
women responded to the questionnaire (74% response rate). Supplementary
information on age at menarche and menopause and postmenopausal
hormone use was obtained in part of the cohort. A follow-up questionnaire
was sent to all 56,030 participants who were still alive and living in the study
area in the autumn of 1997 to update dietary data and to collect
information on other life-style factors, including smoking habits, physical
activity, age at menarche and menopause, use of postmenopausal
hormones, and medical history of diabetes mellitus (additional diabetes
information was obtained by computerized linkage of the cohort with the
National Hospital Discharge Registry). The response rate was 70%. The
study was approved by the Regional Ethical Review Board in Stockholm,
Sweden.
Assessment of diet and covariates. At baseline, a 67-item food
frequency questionnaire (FFQ) was used to assess dietary intake. An
expanded 96-item FFQ was used to update information on dietary intake in
1997. The baseline FFQ has been validated in a subsample of 129 women
randomly chosen from the study population. The Pearson correlation
coefficients (r ) between the FFQ and the mean of 4 1-wk weighted diet
Requests for reprints: Agneta A
˚
kesson, Institute of Environmental Medicine,
Division of Nutritional Epidemiology, Karolinska Institutet, Box 210, 171 77 Stockholm,
Sweden. Phone: 46-8-524-875-42; Fax: 46-8-30-45-71; E-mail: Agneta.Akesson@ki.se.
I2008 American Association for Cancer Research.
doi:10.1158/0008-5472.CAN-08-0329
www.aacrjournals.org 6435 Cancer Res 2008; 68: (15). August 1, 2008
Research Article
Research.
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