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

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.

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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 Vastmanland counties in ¨
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, Vasterås, 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: Received December 22, 2003. Accepted for publication June 21, 2004.


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

Am J Clin Nutr 2004;80:1353–7. Printed in USA. © 2004 American Society for Clinical Nutrition


The study was approved by the ethics committees of Uppsala University Hospital and the Karolinska Institutet (Stockholm). Information on oral contraceptive use was available for 76% of the women in the cohort.” The questionnaire included 8 specific dairy products: low-fat. if present at all. In addition. the date of mammography examination) to the date of ovarian cancer diagnosis. 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– 4 mo apart. the date of migration out of the study area. Overall. Multivariate models were controlled for age.0 y. age at first delivery. and Œ65 y) portion sizes based on mean values from 5922 d of weighed food records among 213 women. Women were grouped into categories of intake of dairy products and lactose. diet. 21 mucinous. had undergone a bilateral oophorectomy or a hysterectomy with removal of an unknown number of ovaries. 2. we present only the multivariate RRs. less likely to have a history of oral contraceptive use. Such data had previously been obtained only from women in Uppsala County at their mammography examination. Pearson’s correlation coefficients ranged from 0. folate. vegetables. according to intakes of dairy products and lactose. Because results of the age-adjusted analyses did not differ substantially from those based on the full multivariate model. height. a follow-up questionnaire was sent to all surviving cohort members. for each category.5% fat) and regular (3% fat) yogurt. this questionnaire solicited information on age at menarche.4 to 0.5-y period). and history of oral contraceptive and postmenopausal hormone use (response rate: 70%). and butter. 5 clear cell. we identified 266 incident cases of invasive epithelial ovarian cancer. reproductive factors. In an analysis of cancers of the endometrioid. and postmenopausal hormone use did not appreciably alter the results. both overall and by its subtypes (serous and nonserous tumors). women who consumed 4 servings of dairy products/d had a significantly (P for trend 0. and more likely to have a slightly lower body mass index (Table 1). and whole milk. The average age at ovarian cancer diagnosis was 64. low-fat ( 1. we excluded women with implausibly high or low total energy intake estimates (ie. we computed the ovarian cancer incidence rate by dividing the number of cases of ovarian cancer by the person-time of follow-up. or 30 June 2003. and intakes of fruit. Thus. 53– 65. are shown in Table 2. Statistical analysis We calculated the follow-up time for each participant from the entry to the cohort (ie. by linkage with the Swedish Inpatient Register. ice cream. 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). Further adjustment for intakes of dietary fat. the date of death from any cause. alcohol. All reported P values are from two-sided tests. mucinous. In 1997. never. fruit. 95% CI: 1. vitamin C. education level. and fish did not materially alter the results (data not shown). before baseline. including 125 serous. for other tumors. their response to the questionnaire constituted the participants’ informed consent. Women chose from 8 possible response categories that ranged from “never/seldom” to “ 4 times/d. 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. and missing. We conducted tests for linear trend across categories by modeling the median values of each category as a continuous variable. and total energy.6 for individual dairy products. cheese. body mass index (in kg/m2). We used Cox proportional hazards models to estimate hazard rate ratios (RRs).6. medium-fat. a total of 61 084 women remained for the analysis.1354 LARSSON ET AL central Sweden agreed to participate in a mammography screening program and completed a questionnaire that elicited information on weight. oral contraceptive use. age at menopause. parity. after control for established and potential risk factors. To calculate nutrients. the multivariate RRs (adjusted for the same variables as in Table 2) . and vegetables increased across the categories of dairy product consumption. parity. vitamin E. we used age-specific (53. 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.02) greater risk (RR: 1. Dietary assessment A food-frequency questionnaire with 67 food items was sent to women in 1987–1990 to assess usual dietary intake during the past 6 mo. Because further adjustment for family history of breast cancer. and clear cell subtypes combined (n 74 cases). we identified and excluded all women who. For the present analysis. the date of a bilateral oophorectomy or a hysterectomy with an unknown number of ovaries removed. and family history of breast cancer. 2011 During 823 572 person-years of follow-up (61 084 women over an average 13. Intakes of total energy. education level. Women who reported a higher consumption of dairy products were more likely to have an education level of 12 y. therefore all analyses are based on all women. Nutrient intake was adjusted for total energy intake by the residual approach (22).1. The median consumption of total dairy products in the highest consumption categories was 3 times that in the lowest consumption categories.ajcn. we did not include those data in the final multivariate model. After these exclusions. Exclusions of women with missing data for oral contraceptives did not essentially change the by guest on October 22. defined as the incidence rate in a particular exposure category divided by the incidence rate in the lowest category. whichever occurred first. 3 SD below or above the mean value for log-transformed energy) and women who had a previously diagnosed cancer (except nonmelanomatous skin cancer). 48 endometrioid. The multivariate RRs of invasive epithelial ovarian cancer.5) of ovarian cancer than did women who consumed 2 servings/d (Table 2). meat. The apparent increase in ovarian cancer risk associated with higher dairy product consumption was strong for tumors of the serous subtype and weak. The Swedish Cancer Register system covers Œ98% of all newly diagnosed cancers in Sweden (21). RESULTS Downloaded from www. oral contraceptive use was coded as ever. and 67 other or unknown histologic subtypes.

3 (0.1.9 (0.1 to 2 2 P for trend4 Total yogurt (servings/d)5 Never or seldom (1 serving wk) 1 1 P for trend3 Cheese (servings/d)5 1 1 to 2 2 P for trend4 3 of 1 glass of daily consumption of total milk.2 (0.9. of cases 24 37 30 34 RR (95% CI) 1.7) 0.9 11 89.6.0 (0. high school.5. AND OVARIAN CANCER TABLE 1 Baseline characteristics of 61 084 women in the Swedish Mammography Cohort according to category of total dairy product consumption1 Categories of total dairy product consumption1 2 to 3 servings/d (n 17 311) 53.8 24.7) 2.8 (0.6 (0.5 1.1. 2. 2011 for increasing categories of dairy product consumption were 1.9. and whole milk. and 1.2.7) 1.1 (0. low-fat milk. 5 clear cell tumors.0 24. and ice cream.7 (0.3) 1.22 0.001 0.1. LACTOSE.0).3) 1.1 (0. 1.0 ( 10 88. At baseline (entry into the cohort between 1987 and 1990).8 12 89.5) 0.2 1355 Characteristic Age at baseline (y) BMI (kg/m2) Education 12 y (%) Ever had children (%) Ever taken oral contraceptives (%)4 Ever taken postmenopausal hormones (%)4 Dietary intake Total energy (kcal/d) Fruit (servings/d) Vegetables (servings/d) 1 2 2 servings/d (n 16 318) 53.0) 1. each increment TABLE 2 Invasive epithelial ovarian cancer according to consumption of dairy products1 All invasive epithelial tumors Intake Total dairy (servings/d) 2 2 to 3 3 to 4 4 P for trend4 Total milk (servings/d)5 Never or seldom ( 1 serving wk) 1 (95% CI: 1.0 1. total yogurt.8) 0.7).org by guest on October 22.55).6.1 1. and 3 children).0 13 89.1.20 0. medium-fat.9 53 53 1645 1.5) 0. BMI (kg/m2.8. and whole milk corresponded to serous ovarian cancer RRs of 1. In analyses of milk modeled in continuous form.0 0. P values (two-sided) were from the chi-square tests (categorical variables) or univariate linear regression models (continuous variables).3 P2 0.73 24. oral contraceptive use (ever or never).70 1. P for trend 0. Among the individual dairy products consumed.15 1. vegetable.2 4 servings/d (n 12 437) 53.8.4) 0.7 294 1.69 Other epithelial tumors2 No.02 1.2 3 to 4 servings/d (n 15 018) 53.3 56 53 1073 1.8) 1. 2.6.0) 1. 1.001 0.0 (0.1.7. Yogurt consumption showed a modest but Serous epithelial tumors No.1) 0.3 (95% CI: 0.4 (0.2 (0.0 1.04 1.1 (1.1.2 53 54 1406 1.0. medium-fat.9.6 3.27 1.0 1.11 1.8. .6).9 (0.06 1.5.1) 0.1. 7% of the study population never or seldom consumed milk.7 303 1.2 (95% CI: 1. and ice cream. education level (ie. total yogurt (low-fat and regular yogurt).9) 2.7) (0.9) 0.4).6 1.6 9.6. Downloaded from www.8 301 1.0 (1.76 1.5).0 (1.15 No.6) 1.1.5. 4 Two-sided P values for trend were calculated with the Wald statistic by using the median values for each category.1.4 (0.9.0 55 54 86 71 18 22 49 36 37 32 37 35 118 66 82 48 36 41 70 30 41 81 107 78 36 55 34 45 52 44 1 Multivariate rate ratios (RRs) were adjusted for age (in 5-y categories). cheese.9.001 0.001 0.9 364 1. and 1.2 (95% CI: 0. nulliparous.7.2 (0.9 (0.2.1. 1.001 Based on 7 major dairy products: low-fat.3 (0.9) 0.42 1.0) 1.0 (0.9 9. 3 Total dairy products included total milk (low-fat. milk showed the strongest positive association with serous ovarian cancer risk.0 1.1 1.7) 0. 2.1.4 9.2 54 53 1254 1.1.2 (95% CI: 1.3) 1.1.1 1. 1.6) 0. of cases 61 71 65 69 RR (95% CI) 1.7) 1.2. and cheese were mutually adjusted.7. parity (ie.1.MILK.2 (0.4 (0.3 (0.9.3) 1.1 (0. low-fat and regular yogurt.7.2 1.5 (0. respectively.6 (0.4 1.8) 1.2) 0.6 (1.2. 1–2. 1.7 3.6. and 67 undifferentiated tumors or tumors of unknown histologic subtypes. 1.8 9. 5 Total milk.9 4.3.ajcn. less than high school.2.7.9) 2. 3 x SD (all such values) 4 Data are based only on those subjects for whom this information was available. 21 mucinous tumors. of cases 37 34 35 35 RR (95% CI) 1. and whole milk). and total energy intakes.6.001 0.5 1.6) 1.0 0. 2 Includes 48 endometrioid tumors.001 0.7 24.0 (reference). and college).2.0 1. in quartiles). and quartiles of fruit.0 (95% CI: 0. cheese.

0. 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. The results were virtually identical when the individual dairy products were included in the model separately. of positive associations for whole milk (4 – 6). yogurt (7). 1.8 g/d. respectively.0 (95% CI: 0.2.3) and 1. vegetable. those with an intake of 2. 16. In the Iowa Women’s Health Study. In the present study and in the Nurses’ Health Study (11). which included 301 cases of epithelial ovarian cancer. Moreover. in which 139 cases of epithelial ovarian cancer were diagnosed among postmenopausal women. less than high school. 7. Kushi et al (10) found that women who drank Œ1 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. and 3 children). education level (ie. and quartiles of fruit.0. milk was the major source.2.8.ajcn.2 7. contributing approximately two-thirds of total lactose intake. and cottage cheese (7). the associations with specific subtypes of ovarian cancer were not examined. Lactose intake showed a linear positive association with the risk of serous ovarian cancer (P for trend 0. there was no association with other ovarian cancer subtypes (11). 2011 . In the case-control studies.7 g/d) quartiles of lactose intake were compared. 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. By contrast. corresponding to the amount usually added to 1–2 cups of coffee or tea) were less than half (0. Five case-control studies to date have related total consumption of dairy products to the risk of ovarian cancer (5. Multivariate rate ratios for invasive serous epithelial ovarian cancer according to lactose intake.0 (95% CI: 0.65). ice cream.6). 1. is unlikely to explain the absence of association in all case-control studies. The corresponding RRs for total ovarian cancer and nonserous tumors was 1. none of those studies showed any significant association. population-based. and that association was restricted to women with low activity of galactose-1-phosphate uridyltransferase. 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. cheese.9. 1.1 (95% CI: 0. Figure 1). women who consumed 5 servings of yogurt/wk had a risk of serous ovarian cancer 2. 1. oral contraceptive use (ever or never). 95% CI: 0. DISCUSSION In this large. in quartiles). 26). parity (ie. and college).2 g/d) and the bottom (7. 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. 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. Women who consumed Œ1 glass of milk/d had double the risk of serous ovarian cancer compared with women who never or seldom drank milk.11).4) to 1. The average lactose intake in the cohort was 12. a lack of association in some previous studies might be due to the fact that specific ovarian cancer subtypes were not studied. 95% CI: 1. Harlow et al (12) hypothesized that galactose—a component sugar of the disaccharide lactose—might increase the risk of Downloaded from www. which would lead to a spurious inverse association with low-fat milk consumption and a positive association with whole milk consumption. 23–25).3). nonsignificant positive relation with the risk of serous ovarian cancer (P for trend 0.8. and cheese (28).9) as likely to develop serous ovarian cancer. and of inverse associations for total milk (27). 9).4. 1–2.006. They further observed a nonsignificant (60%) increase in the risk of total ovarian cancer when the top (25.0. 3– 4 tablespoons. For each 11-g increment in daily lactose intake. the risk of serous ovarian cancer increased by 20%.1356 LARSSON ET AL FIGURE 1. nulliparous.1. prospective cohort study of Swedish women. However. ie. 95% CI: 0. The median lactose intake in the reference group ( ) was 20 g/d. Values were adjusted for age (in 5-y categories). ie.5 g/d (the amount of lactose in 50 g milk. were significantly positively associated with the risk of serous ovarian cancer. without mutual adjustment (data not shown).9. 8. The association between lactose intake and ovarian cancer risk has been considered in many case-control studies (5. an enzyme involved in the galactose (a component sugar of lactose) metabolic pathway. 1. 8. 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. 8.4 times that of women who almost never consumed yogurt. BMI (kg/m2. Recall bias. the associations with dairy products (milk and yogurt) and lactose intake were restricted to the serous subtype.2 (95% CI: 1. In the report of Fairfield et al (11) from the Nurses’ Health Study. particularly milk.2). however.5). Relative to women with a lactose intake of 15 g/d (corresponding to the amount of lactose in 1–2 glasses of milk). skim or low-fat milk (4 – 6. and total energy intakes. high school. only 1 (7) of these 8 studies provided evidence of a positive association between lactose intake and ovarian cancer risk. 1. 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). 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. When we included intakes of lactose and milk simultaneously in the multivariate model (Pearson’s correlation coefficient: r 0. Milk and yogurt were the major sources of lactose in our study population. 13–17). When lactose was analyzed as a continuous variable. and butter were not associated with the risk of ovarian cancer overall or of its subtypes. which corresponds to 2 glasses milk/d. intakes of lactose and dairy products. Alternatively. whereas the relative risk for increments of lactose intake was essentially unaltered (RR for each 10 g/d increment: by guest on October 22.

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