domingo, 19 de febrero de 2012

Leche cáncer ovarios

Milk and lactose intakes and ovarian cancer risk in the Swedish
Mammography Cohort1–3
Susanna C Larsson, Leif Bergkvist, and Alicja Wolk
ABSTRACT
Background: High intakes of dairy products and of the milk sugar
lactose have been hypothesized to increase ovarian cancer risk, but
prospective data are scarce.
Objective: We examined the association between intakes of dairy
products and lactose and the risk of total epithelial ovarian cancer
and its subtypes.
Design: This was a prospective population-based cohort study of
61 084 women aged 38–76 y who were enrolled in the Swedish
Mammography Cohort. Diet was assessed in 1987–1990 with the
use of a self-administered food-frequency questionnaire. During an
average follow-up of 13.5 y, 266 women were diagnosed with invasive
epithelial ovarian cancer; 125 of those women had serous
ovarian cancer.
Results: After adjustment for potential confounders, women who
consumed 4 servings of total dairy products/d had a risk of serous
ovarian cancer (rate ratio: 2.0; 95% CI: 1.1, 3.7; P for trend 0.06)
twice that of women who consumed 2 servings/d. No significant
association was found for other subtypes of ovarian cancer. Milk was
the dairy product with the strongest positive association with serous
ovarian cancer (rate ratio comparing consuming 2 glasses milk/d
with consuming milk never or seldom: 2.0; 95% CI: 1.1, 3.7; P for
trend 0.04). We observed a positive association between lactose
intake and serous ovarian cancer risk (P for trend 0.006).
Conclusions: Our data indicate that high intakes of lactose and dairy
products, particularly milk, are associated with an increased risk of
serous ovarian cancer but not of other subtypes of ovarian cancer.
Future studies should consider ovarian cancer subtypes
separately. Am J Clin Nutr 2004;80:1353–7.
KEY WORDS Ovarian cancer, milk, lactose, galactose, diet,
epidemiology, cohort studies
INTRODUCTION
The strong correlation between national per capita milk consumption
in the United States and the national incidence and
mortality rates of ovarian cancer raised the hypothesis that consumption
of milk and other dairy products may increase the risk
of this malignancy (1–3). Analytic epidemiologic studies investigating
this hypothesis have, however, yielded conflicting results.
Frequent consumption of whole milk (4–6), yogurt (7), and
cheese (7) has been associated with an increased risk of ovarian
cancer in some case-control studies. In contrast, evidence suggests
a decreased risk of ovarian cancer associated with higher
consumption of skim or low-fat milk (4–6, 8, 9). To date, only 2
prospective cohort studies have examined the possibility of an
association of the consumption of milk and other dairy products
with the incidence of ovarian cancer. In the Iowa Women’s
Health Study, women who reported a high consumption of total
dairy products, skim milk, and cheese had a higher risk of ovarian
cancer than did those who rarely consumed these foods (10). The
Nurses’ Health Study found a positive association between consumption
of skim or low-fat milk and yogurt and the risk of
ovarian cancer, and the findings further suggested that the association
might be confined to serous ovarian cancer (11).
Dairy products are the major source of galactose, a component
sugar of lactose that may increase ovarian cancer risk by direct
toxicity to oocytes or by elevating gonadotropin concentrations,
thereby stimulating proliferation of ovarian epithelium (12). A
positive association between lactose intake and the risk of ovarian
cancer was observed in the Iowa Women’s Health Study (10)
and in the Nurses’ Health Study (11), but not in any of 7 casecontrol
studies (5, 8, 13–17).
Given the paucity of prospective data on the intakes of dairy
products and of lactose in relation to the incidence of total epithelial
ovarian cancer and especially ovarian cancer subtypes, we
examined this topic in a large, population-based, prospective
cohort study in Sweden. That country has one of the highest rates
of ovarian cancer in the world (18), and it citizens consume a
wide range of dairy products.
SUBJECTS AND METHODS
Study population
The design of the Swedish Mammography Cohort has been
described in detail elsewhere (19). In brief, the cohort was established
between 1987 and 1990, when 66 651 women aged
38–76 y and residing in Uppsala and Va¨stmanland counties in
1 From the Division of Nutritional Epidemiology, The National Institute of
Environmental Medicine, Karolinska Institutet, Stockholm (SCL and AW),
and the Department of Surgery and the Center for Clinical Research, Uppsala
University, Central Hospital, Va¨sterås, Sweden (LB).
2 Supported by research grants from the Swedish Research Council/Longitudinal
Studies and the Swedish Cancer Foundation.
3 Reprints not available. Address correspondence to SC Larsson, Division
of Nutritional Epidemiology, The National Institute of Environmental Medicine,
Karolinska Institutet, Box 210, SE-171 77 Stockholm, Sweden. Email:
susanna.larsson@imm.ki.se.
Received December 22, 2003.
Accepted for publication June 21, 2004.
Am J Clin Nutr 2004;80:1353–7. Printed in USA. © 2004 American Society for Clinical Nutrition 1353
central Sweden agreed to participate in a mammography screening
program and completed a questionnaire that elicited information
on weight, height, education level, diet, parity, age at first
delivery, and family history of breast cancer. In 1997, a follow-up
questionnaire was sent to all surviving cohort members; this
questionnaire solicited information on age at menarche, age at
menopause, and history of oral contraceptive and postmenopausal
hormone use (response rate: 70%). Such data had previously
been obtained only from women in Uppsala County at their
mammography examination.
For the present analysis, we excluded women with implausibly
high or low total energy intake estimates (ie, 3 SD below or
above the mean value for log-transformed energy) and women
who had a previously diagnosed cancer (except nonmelanomatous
skin cancer). In addition, by linkage with the Swedish Inpatient
Register, we identified and excluded all women who,
before baseline, had undergone a bilateral oophorectomy or a
hysterectomy with removal of an unknown number of ovaries.
After these exclusions, a total of 61 084 women remained for the
analysis. The study was approved by the ethics committees of
Uppsala University Hospital and the Karolinska Institutet
(Stockholm); their response to the questionnaire constituted the
participants’ informed consent.
Dietary assessment
Afood-frequency questionnaire with 67 food items was sent to
women in 1987–1990 to assess usual dietary intake during the
past 6 mo.Womenchose from 8 possible response categories that
ranged from “never/seldom” to “ 4 times/d.” The questionnaire
included 8 specific dairy products: low-fat, medium-fat, and
whole milk; low-fat ( 1.5% fat) and regular (3% fat) yogurt;
cheese; ice cream; and butter. To calculate nutrients, we used
age-specific ( 53, 53–65, and 65 y) portion sizes based on
mean values from 5922 d of weighed food records among 213
women. We estimated nutrient intakes by multiplying the consumption
frequency of each food by portion size and nutrient
content (/100 g) and by using composition values from the Swedish
National Food Administration Database (20).
The validity of the dietary questionnaire was evaluated in a
random sample of 129 women from the cohort by comparing the
questionnaire with data from four 1-wk dietary records collected
3–4mo apart. Pearson’s correlation coefficients ranged from 0.4
to 0.6 for individual dairy products.
Identification of ovarian cancer cases and follow-up of
the cohort
Incident ovarian cancer cases that occurred in the cohort from
March 1987 through June 2003 were identified by linkage of the
study population with 2 independent sources: the national Swedish
Cancer Registry and the Regional Cancer Registry covering
the study area. The Swedish Cancer Register system covers 98%
of all newly diagnosed cancers in Sweden (21). We ascertained
dates of deaths and dates when a participant moved out from the
study area by matching the cohort with the Swedish Death Registry
and the Swedish Population Registry.
Statistical analysis
Wecalculated the follow-up time for each participant from the
entry to the cohort (ie, the date of mammography examination) to
the date of ovarian cancer diagnosis, the date of a bilateral oophorectomy
or a hysterectomy with an unknown number of ovaries
removed, the date of death from any cause, the date of
migration out of the study area, or 30 June 2003, whichever
occurred first. Women were grouped into categories of intake of
dairy products and lactose; for each category, we computed the
ovarian cancer incidence rate by dividing the number of cases of
ovarian cancer by the person-time of follow-up. We used Cox
proportional hazards models to estimate hazard rate ratios (RRs),
defined as the incidence rate in a particular exposure category
divided by the incidence rate in the lowest category. Multivariate
models were controlled for age, body mass index (in kg/m2),
education level, parity, oral contraceptive use, and intakes of
fruit, vegetables, and total energy. Because further adjustment
for family history of breast cancer, reproductive factors, and
postmenopausal hormone use did not appreciably alter the results,
we did not include those data in the final multivariate
model. Information on oral contraceptive use was available for
76%of thewomenin the cohort. Thus, oral contraceptive use was
coded as ever, never, and missing. Exclusions of women with
missing data for oral contraceptives did not essentially change
the results; therefore all analyses are based on all women.
Nutrient intake was adjusted for total energy intake by the
residual approach (22). We conducted tests for linear trend
across categories by modeling the median values of each
category as a continuous variable. All reported P values are
from two-sided tests.
RESULTS
During 823 572 person-years of follow-up (61 084 women
over an average 13.5-y period), we identified 266 incident cases
of invasive epithelial ovarian cancer, including 125 serous, 48
endometrioid, 21 mucinous, 5 clear cell, and 67 other or unknown
histologic subtypes. The average age at ovarian cancer diagnosis
was 64.0 y. The median consumption of total dairy products in
the highest consumption categories was 3 times that in the lowest
consumption categories. Women who reported a higher consumption
of dairy products were more likely to have an education
level of 12 y, less likely to have a history of oral contraceptive
use, and more likely to have a slightly lower body mass index
(Table 1). Intakes of total energy, fruit, and vegetables increased
across the categories of dairy product consumption.
The multivariate RRs of invasive epithelial ovarian cancer,
both overall and by its subtypes (serous and nonserous tumors),
according to intakes of dairy products and lactose, are shown in
Table 2. Because results of the age-adjusted analyses did not
differ substantially from those based on the full multivariate
model, we present only the multivariate RRs. Overall, after control
for established and potential risk factors, women who consumed
4 servings of dairy products/d had a significantly (P for
trend 0.02) greater risk (RR: 1.6; 95% CI: 1.1, 2.5) of ovarian
cancer than did women who consumed 2 servings/d (Table 2).
Further adjustment for intakes of dietary fat, folate, vitamin C,
vitamin E, alcohol, meat, and fish did not materially alter the
results (data not shown). The apparent increase in ovarian cancer
risk associated with higher dairy product consumption was
strong for tumors of the serous subtype and weak, if present at all,
for other tumors. In an analysis of cancers of the endometrioid,
mucinous, and clear cell subtypes combined (n 74 cases), the
multivariate RRs (adjusted for the same variables as in Table 2)
1354 LARSSON ET AL
for increasing categories of dairy product consumption were 1.0
(reference), 1.0 (95% CI: 0.5, 2.0), 1.2 (95% CI: 0.6, 2.5), and 1.2
(95% CI: 0.6, 2.6; P for trend 0.55).
Among the individual dairy products consumed, milk showed
the strongest positive association with serous ovarian cancer risk.
In analyses of milk modeled in continuous form, each increment
of 1 glass of daily consumption of total milk, low-fat milk, and
whole milk corresponded to serous ovarian cancer RRs of 1.2
(95% CI: 1.0, 1.4), 1.2 (95% CI: 1.0, 1.6), and 1.3 (95% CI: 0.9,
1.7), respectively. At baseline (entry into the cohort between
1987 and 1990), 7% of the study population never or seldom
consumed milk. Yogurt consumption showed a modest but
TABLE 1
Baseline characteristics of 61 084 women in the Swedish Mammography Cohort according to category of total dairy product consumption1
Characteristic
Categories of total dairy product consumption1
P2
2 servings/d
(n 16 318)
2 to 3
servings/d
(n 17 311)
3 to 4
servings/d
(n 15 018)
4 servings/d
(n 12 437)
Age at baseline (y) 53.6 9.73 53.8 9.7 53.9 9.8 53.4 9.8 0.20
BMI (kg/m2) 24.9 4.0 24.7 3.9 24.6 3.8 24.6 3.8 0.001
Education 12 y (%) 10 11 12 13 0.001
Ever had children (%) 88.3 89.2 89.2 89.9 0.001
Ever taken oral contraceptives (%)4 56 54 53 53 0.001
Ever taken postmenopausal hormones (%)4 53 53 54 53 0.22
Dietary intake
Total energy (kcal/d) 1073 303 1254 294 1406 301 1645 364 0.001
Fruit (servings/d) 1.4 1.1 1.5 1.1 1.5 1.1 1.6 1.2 0.001
Vegetables (servings/d) 1.7 1.2 1.7 1.2 1.8 1.2 1.9 1.3 0.001
1 Based on 7 major dairy products: low-fat, medium-fat, and whole milk; low-fat and regular yogurt; cheese; and ice cream.
2 P values (two-sided) were from the chi-square tests (categorical variables) or univariate linear regression models (continuous variables).
3 x SD (all such values)
4 Data are based only on those subjects for whom this information was available.
TABLE 2
Invasive epithelial ovarian cancer according to consumption of dairy products1
Intake
All invasive epithelial tumors Serous epithelial tumors Other epithelial tumors2
No. of cases RR (95% CI) No. of cases RR (95% CI) No. of cases RR (95% CI)
Total dairy (servings/d)3
2 61 1.0 24 1.0 37 1.0
2 to 3 71 1.2 (0.9,1.7) 37 1.6 (0.9,2.7) 34 1.0 (0.6,1.6)
3 to 4 65 1.4 (0.9,2.0) 30 1.6 (0.9,2.9) 35 1.2 (0.7,2.0)
4 69 1.6 (1.1,2.5) 34 2.0 (1.1,3.7) 35 1.4 (0.8,2.4)
P for trend4 0.02 0.06 0.15
Total milk (servings/d)5
Never or seldom ( 1 serving wk) 55 1.0 18 1.0 37 1.0
1 54 1.2 (0.9,1.8) 22 1.5 (0.8,2.9) 32 1.1 (0.7,1.8)
1.1 to 2 86 1.2 (0.9,1.8) 49 2.1 (1.2,3.7) 37 0.8 (0.5,1.3)
2 71 1.3 (0.9,1.9) 36 2.0 (1.1,3.7) 35 1.0 (0.6,1.6)
P for trend4 0.27 0.04 0.70
Total yogurt (servings/d)5
Never or seldom ( 1 serving wk) 118 1.0 48 1.0 70 1.0
1 66 1.0 (0.7,1.3) 36 1.3 (0.8,2.0) 30 0.7 (0.5,1.1)
1 82 1.1 (0.8,1.5) 41 1.4 (0.9,2.2) 41 0.9 (0.6,1.4)
P for trend3 0.42 0.11 0.76
Cheese (servings/d)5
1 81 1.0 36 1.0 45 1.0
1 to 2 107 0.9 (0.7,1.3) 55 1.0 (0.7,1.6) 52 0.9 (0.6,1.3)
2 78 1.2 (0.9,1.7) 34 1.1 (0.7,1.9) 44 1.3 (0.8,2.1)
P for trend4 0.17 0.69 0.15
1 Multivariate rate ratios (RRs) were adjusted for age (in 5-y categories), BMI (kg/m2; in quartiles), education level (ie, less than high school, high school,
and college), parity (ie, nulliparous, 1–2, and 3 children), oral contraceptive use (ever or never), and quartiles of fruit, vegetable, and total energy intakes.
2 Includes 48 endometrioid tumors, 21 mucinous tumors, 5 clear cell tumors, and 67 undifferentiated tumors or tumors of unknown histologic subtypes.
3 Total dairy products included total milk (low-fat, medium-fat, and whole milk), total yogurt (low-fat and regular yogurt), cheese, and ice cream.
4 Two-sided P values for trend were calculated with the Wald statistic by using the median values for each category.
5 Total milk, total yogurt, and cheese were mutually adjusted.
MILK, LACTOSE, AND OVARIAN CANCER 1355
nonsignificant positive relation with the risk of serous ovarian
cancer (P for trend 0.11). By contrast, cheese, ice cream, and
butter were not associated with the risk of ovarian cancer overall
or of its subtypes. The results were virtually identical when the
individual dairy products were included in the model separately,
ie, without mutual adjustment (data not shown).
Lactose intake showed a linear positive association with the
risk of serous ovarian cancer (Pfor trend 0.006; Figure 1). The
average lactose intake in the cohort was 12.2 7.8 g/d; milk was
the major source. Relative to women with a lactose intake of 15
g/d (corresponding to the amount of lactose in 1–2 glasses of
milk), those with an intake of 2.5 g/d (the amount of lactose in
50 g milk, ie, 3–4 tablespoons, corresponding to the amount
usually added to 1–2 cups of coffee or tea) were less than half
(0.4; 95% CI: 0.1, 0.9) as likely to develop serous ovarian cancer.
When lactose was analyzed as a continuous variable, each 10 g/d
increase in lactose intake (the amount of lactose in 1 glass milk)
was associated with a 20% greater risk of serous ovarian cancer
(multivariate RR: 1.2; 95% CI: 1.0, 1.5). The corresponding RRs
for total ovarian cancer and nonserous tumors was 1.1 (95% CI:
0.9, 1.3) and 1.0 (95% CI: 0.8, 1.2), respectively.
When we included intakes of lactose and milk simultaneously
in the multivariate model (Pearson’s correlation coefficient: r
0.65), the observed positive association between total milk consumption
and the risk of serous ovarian cancer was mostly confined
to lactose intake because the relative risk for each 1 glass/d
increment in total milk consumption decreased from 1.2 (95%
CI: 1.0, 1.4) to 1.0 (95% CI: 0.8, 1.3), whereas the relative risk for
increments of lactose intake was essentially unaltered (RR for
each 10 g/d increment: 1.2; 95% CI: 0.9, 1.6).
DISCUSSION
In this large, population-based, prospective cohort study of
Swedish women, intakes of lactose and dairy products, particularly
milk, were significantly positively associated with the risk
of serous ovarian cancer. Women who consumed 1 glass of
milk/d had double the risk of serous ovarian cancer compared
with women who never or seldom drank milk.
The results of our cohort study are broadly consistent with
findings from the Iowa Women’s Health Study (10) and the
Nurses’ Health Study (11). In the Iowa Women’s Health Study,
in which 139 cases of epithelial ovarian cancer were diagnosed
among postmenopausal women, Kushi et al (10) found that
women who drank 1 glass of skim milk/d had a 73% greater
risk of total ovarian cancer than did those who drank 1 glass of
skim milk/wk. They further observed a nonsignificant (60%)
increase in the risk of total ovarian cancer when the top (25.2 g/d)
and the bottom ( 7.7 g/d) quartiles of lactose intake were compared;
the associations with specific subtypes of ovarian cancer
were not examined. In the report of Fairfield et al (11) from the
Nurses’ Health Study, which included 301 cases of epithelial
ovarian cancer, those authors documented a 69% greater risk of
serous ovarian cancer in women who consumed 1 glasses of
skim or low-fat milk/d than in women who almost never drank
milk. Moreover, women who consumed 5 servings of yogurt/
wk had a risk of serous ovarian cancer 2.4 times that of
women who almost never consumed yogurt. For each 11-g increment
in daily lactose intake, the risk of serous ovarian cancer
increased by 20%; there was no association with other ovarian
cancer subtypes (11).
Five case-control studies to date have related total consumption
of dairy products to the risk of ovarian cancer (5, 8, 23–25);
none of those studies showed any significant association. Findings
for the association of individual dairy products with ovarian
cancer risk have been conflicting: there have been reports of no
association for any dairy product (15, 16, 26); of positive associations
for whole milk (4–6), yogurt (7), and cottage cheese (7);
and of inverse associations for total milk (27), skim or low-fat
milk (4–6, 8, 9), and cheese (28). The association between lactose
intake and ovarian cancer risk has been considered in many
case-control studies (5, 7, 8, 13–17). However, only 1 (7) of these
8 studies provided evidence of a positive association between
lactose intake and ovarian cancer risk, and that association was
restricted to women with low activity of galactose-1-phosphate
uridyltransferase, an enzyme involved in the galactose (a component
sugar of lactose) metabolic pathway.
One possible explanation for the discrepancy between cohort
studies and case-control studies with respect to the association
between consumption of dairy products and ovarian cancer risk
may have to do with the retrospective design of the latter type of
studies. In the case-control studies, recall bias might have been
introduced by overestimation of consumption of skim or low-fat
milk and underestimation of consumption of whole milk by controls,
which would lead to a spurious inverse association with
low-fat milk consumption and a positive association with whole
milk consumption. Recall bias, however, is unlikely to explain
the absence of association in all case-control studies. Alternatively,
a lack of association in some previous studies might be due
to the fact that specific ovarian cancer subtypes were not studied.
In the present study and in the Nurses’ Health Study (11), the
associations with dairy products (milk and yogurt) and lactose
intake were restricted to the serous subtype.
We can only speculate about possible mechanisms for the
observed increased risk of ovarian cancer associated with high
intakes of dairy products (milk and yogurt) and lactose. Milk and
yogurt were the major sources of lactose in our study population,
contributing approximately two-thirds of total lactose intake.
Harlow et al (12) hypothesized that galactose—a component
sugar of the disaccharide lactose—might increase the risk of
FIGURE 1. Multivariate rate ratios for invasive serous epithelial ovarian
cancer according to lactose intake. Values were adjusted for age (in 5-y
categories), BMI (kg/m2; in quartiles), education level (ie, less than high
school, high school, and college), parity (ie, nulliparous, 1–2, and 3 children),
oral contraceptive use (ever or never), and quartiles of fruit, vegetable,
and total energy intakes. The median lactose intake in the reference group ( )
was 20 g/d, which corresponds to 2 glasses milk/d.
1356 LARSSON ET AL
ovarian cancer either by direct toxicity to the oocytes or by
inducing high concentrations of gonadotropins, thereby stimulating
the proliferation of the ovarian surface epithelium. Excess
gonadotropin stimulation of the ovaries has been reported in
galactosemic women deficient in the galactose-1-phosphate uridyltransferase
enzyme. Ovaries have an unusually high local
concentration and a high tissue-specific activity of galactose-1-
phosphate uridyltransferase (29), traits that potentially make
them more susceptible to galactose toxicity.
The major strengths of our study include its population-based
design, the relatively large number of cases of this cancer, the
ability to examine specific subtypes of ovarian cancer, and the
completeness of case ascertainment through the Swedish Cancer
Register system. Furthermore, in contrast to most studies on the
relation between diet and ovarian cancer, our study was based on
prospectively collected data, which eliminated bias attributable
to differential recall of food intake by women with and without
cancer. Moreover, our dietary assessments were based on a validated
food-frequency questionnaire that ranked consumption of
dairy products well. Our study is limited by its observational
character; hence, we cannot exclude the possibility that uncontrolled
confounding of our risk estimates by factors that are
unmeasured or not accounted for influenced our results. However,
adjustment for potential dietary and lifestyle confounding
factors did not appreciably alter the results, which suggests
that residual confounding is unlikely to explain our
observed findings.
In conclusion, this prospective cohort study provides evidence
that high intakes of lactose and dairy products, especially milk,
may increase the risk of serous ovarian cancer. Continued research
is warranted to further elucidate the association and mechanisms
for the observed increased risk, and particular focus
should be placed on ovarian cancer subtypes.
The contributions of the authors to the manuscript were as follows: study
concept and design (SCL and AW), data collection (LB and AW), statistical
analyses (SCL), writing the manuscript (SCL), interpreting the results (SCL,
LB, and AW), and critical revision of manuscript (LB and AW). All authors
reviewed the final manuscript. None of the authors had any financial or
personal conflicts of interest.
REFERENCES
1. Cramer DW. Lactase persistence and milk consumption as determinants
of ovarian cancer risk. Am J Epidemiol 1989;130:904 –10.
2. Rose DP, Boyar AP, Wynder EL. International comparisons of mortality
rates for cancer of the breast, ovary, prostate, and colon, and per capita
food consumption. Cancer 1986;58:2363–71.
3. Armstrong B, Doll R. Environmental factors and cancer incidence and
mortality in different countries, with special reference to dietary practices.
Int J Cancer 1975;15:617–31.
4. Cramer DW, Welch WR, Hutchison GB, Willett W, Scully RE. Dietary
animal fat in relation to ovarian cancer risk. Obstet Gynecol 1984;63:
833–8.
5. Webb PM, Bain CJ, Purdie DM, Harvey PW, Green A. Milk consumption,
galactose metabolism and ovarian cancer (Australia). Cancer
Causes Control 1998;9:637– 44.
6. Mettlin CJ, Piver MS.Acase-control study of milk-drinking and ovarian
cancer risk. Am J Epidemiol 1990;132:871– 6.
7. Cramer DW, Harlow BL, Willett WC, et al. Galactose consumption
and metabolism in relation to the risk of ovarian cancer. Lancet
1989;2:66 –71.
8. Goodman MT, Wu AH, Tung KH, et al. Association of dairy products,
lactose, and calcium with the risk of ovarian cancer. Am J Epidemiol
2002;156:148 –57.
9. Bertone ER, Hankinson SE, Newcomb PA, et al. A population-based
case-control study of carotenoid and vitaminAintake and ovarian cancer
(United States). Cancer Causes Control 2001;12:83–90.
10. Kushi LH, Mink PJ, Folsom AR, et al. Prospective study of diet and
ovarian cancer. Am J Epidemiol 1999;149:21–31.
11. Fairfield KM, Hunter DJ, Colditz GA, et al. A prospective study of
dietary lactose and ovarian cancer. Int J Cancer 2004;110:271–7.
12. Harlow BL, CramerDW,Geller J, WillettWC,BellDA,WelchWR.The
influence of lactose consumption on the association of oral contraceptive
use and ovarian cancer risk. Am J Epidemiol 1991;134:445–53.
13. Risch HA, Jain M, Marrett LD, Howe GR. Dietary lactose intake, lactose
intolerance, and the risk of epithelial ovarian cancer in southern Ontario
(Canada). Cancer Causes Control 1994;5:540–8.
14. Herrinton LJ, Weiss NS, Beresford SA, et al. Lactose and galactose
intake and metabolism in relation to the risk of epithelial ovarian cancer.
Am J Epidemiol 1995;141:407–16.
15. Engle A, Muscat JE, Harris RE. Nutritional risk factors and ovarian
cancer. Nutr Cancer 1991;15:239–47.
16. CramerDW,Greenberg ER, Titus-Ernstoff L, et al.Acase-control study
of galactose consumption and metabolism in relation to ovarian cancer.
Cancer Epidemiol Biomarkers Prev 2000;9:95–101.
17. Cozen W, Peters R, Reichardt JK, et al. Galactose-1-phosphate uridyl
transferase (GALT) genotype and phenotype, galactose consumption,
and the risk of borderline and invasive ovarian cancer (United States).
Cancer Causes Control 2002;13:113–20.
18. Parkin DM, Ferlay J, Raymond L, Young J. Cancer incidence in five
continents. Lyon, France: International Agency for Research on Cancer,
1997.
19. Wolk A, Bergstrom R, Hunter D, et al.Aprospective study of association
of monounsaturated fat and other types of fat with risk of breast cancer.
Arch Intern Med 1998;158:41–5.
20. Bergström L, Kylberg E, Hagman U, Erikson H, Bruce Å. The food
composition database KOST: the National Food Administration’s Information
System for nutritive values of food. Vår Föda
1991;43:439–47 (in Swedish).
21. Mattson B, Wallgren A. Completeness of the Swedish Cancer Register.
Non-notified cancer cases recorded on death certificates in 1978. Acta
Radiol Oncol 1984;23:305–13.
22. Willett W, Stampfer MJ. Total energy intake: implications for epidemiologic
analyses. Am J Epidemiol 1986;124:17–27.
23. Salazar-Martinez E, Lazcano-Ponce EC, Gonzalez Lira-Lira G,
Escudero-De los Rios P, Hernandez-Avila M. Nutritional determinants
of epithelial ovarian cancer risk: a case-control study in Mexico. Oncology
2002;63:151–7.
24. Zhang M, Yang ZY, Binns CW, Lee AH. Diet and ovarian cancer risk:
a case-control study in China. Br J Cancer 2002;86:712–7.
25. McCann SE, Freudenheim JL, Marshall JR, Graham S. Risk of human
ovarian cancer is related to dietary intake of selected nutrients, phytochemicals
and food groups. J Nutr 2003;133:1937– 42.
26. Bertone ER, Rosner BA, Hunter DJ, et al. Dietary fat intake and ovarian
cancer in a cohort of US women. Am J Epidemiol 2002;156:22–31.
27. Mori M, Miyake H. Dietary and other risk factors of ovarian cancer
among elderly women. Jpn J Cancer Res 1988;79:997–1004.
28. Bosetti C, Negri E, Franceschi S, et al. Diet and ovarian cancer risk: a
case-control study in Italy. Int J Cancer 2001;93:911–5.
29. Xu YK, Ng WG, Kaufman FR, Lobo RA, Donnell GN. Galactose metabolism
in human ovarian tissue. Pediatr Res 1989;25:151–5.
MILK, LACTOSE, AND OVARIAN CANCER 1357

No hay comentarios:

Publicar un comentario