American Journal of Epidemiology Advance Access originally published online on September 12, 2006
American Journal of Epidemiology 2006 164(10):990-997; doi:10.1093/aje/kwj309
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Original Contribution |
Dietary Fat and Risk of Postmenopausal Breast Cancer in a 20-year Follow-up
1 Harvard School of Public Health, Boston, MA
2 Channing Laboratory, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, MA
Correspondence to Esther Kim, Harvard School of Public Health, 651 Huntington Avenue, Boston, MA 02115 (e-mail: ehjkim{at}hsph.harvard.edu).
Received for publication April 29, 2005. Accepted for publication April 13, 2006.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Dietary fat in midlife has not been associated with breast cancer risk in most studies, but few have followed women beyond one decade. The authors examined the relation of dietary fat, assessed by repeated questionnaires, to incidence of postmenopausal breast cancer in a cohort of 80,375 US women (3,537 new cases) prospectively followed for 20 years between 1980 and 2000. The multivariable relative risk for an increment of 5% of energy from total dietary fat intake was 0.98 (95% confidence interval: 0.95, 1.00). Additionally, specific types of fat were not associated with an increased risk of breast cancer. Furthermore, secondary analyses indicated no differences in breast cancer risk by estrogen receptor or progesterone receptor status. However, stratification by waist circumference indicated a significant decrease in breast cancer risk for participants with a waist circumference of 35 inches (88.9 cm) or greater (p-trend = 0.04). None of the latency intervals investigated were associated with an increased risk of breast cancer. In addition, fat intake before menopause was not related to risk of postmenopausal breast cancer. These results suggest a reduction in breast cancer risk for women with insulin resistance syndrome who consume high-fat diets and no association between specific sources of fat during midlife and risk of postmenopausal breast cancer.
breast neoplasms; dietary fats; postmenopause
Abbreviations: CI, confidence interval; FFQ, food frequency questionnaire
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Most ecologic studies and some case-control studies suggest a positive association between a high-fat diet and breast cancer risk (1
–4). However, dietary fat in midlife has not been associated with breast cancer risk in most prospective studies, nor was an association found in a pooled analysis of prospective studies with over 7,000 breast cancer cases (5). In an earlier analysis of the Nurses' Health Study cohort with 14 years follow-up, no evidence of a positive association was seen between an increase of 5 percent of energy derived from total fat and breast cancer risk (relative risk = 0.97, 95 percent confidence interval (CI): 0.94, 1.00); the overall trend was weakly inverse (p-trend = 0.03) (6). An inverse association might be explained by the adverse metabolic effects of low-fat/high-carbohydrate diets among persons with greater insulin resistance (7, 8). Also, some animal and epidemiologic research suggests that greater intake of monounsaturated fats or omega-3 fatty acids might reduce risk of breast cancer (6, 9–13).
In a recent report from the Women's Health Initiative, participants assigned to a low-fat dietary intervention did not experience a significant decrease in breast cancer risk during 8 years of follow-up (relative risk = 0.91, 95 percent CI: 0.83, 1.01) (14). However, in a post hoc analysis, women assigned to the low-fat diet were found to have a significantly lower risk of breast cancers with positive estrogen receptors and negative progesterone receptors.
One limitation of previous studies—including the Women's Health Initiative, which had an average of 8 years of follow-up—has been that a long latency may exist between the intake of fat and the diagnosis of breast cancer. Additionally, in a recent study of young women from the Nurses' Health Study II cohort, greater intake of animal fat before menopause was associated with an increased risk of breast cancer (15). However, participants in Nurses' Health Study II were much younger, and only 10 percent of the cases occurred in postmenopausal women.
The extended follow-up of the Nurses' Health Study cohort provides an opportunity to address the issue of a long latency between fat intake and breast cancer risk. In this analysis of 80,375 postmenopausal women followed for 20 years, we sought to address some of the questions raised by previous work. We examined specific types of fat and stratified our analyses by waist circumference and body mass index as proxies for insulin resistance. In addition, we conducted analyses of tumors classified by estrogen and progesterone receptor status. We also examined the impact of premenopausal fat intake on postmenopausal breast cancer risk, which to our knowledge has not been done previously.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Study population
Established in 1976, the Nurses' Health Study is a prospective cohort study consisting of 121,701 US registered nurses aged 30–55 years at baseline. At enrollment, women completed a mailed questionnaire regarding their medical histories and lifestyles. Follow-up questionnaires are mailed every 2 years in order to update information on participants' health and lifestyle. In 1980, a 61-item food frequency questionnaire (FFQ) was added, and in 1984 and subsequently, the FFQ was expanded to include approximately 130 items. For our analyses, we excluded women who did not complete the 1980 dietary questionnaire, reported an energy intake of less than 500 kcal/day or greater than 3,500 kcal/day, or left more than 10 food items blank, as well as women with a previous diagnosis of cancer. We limited the analysis to women who were postmenopausal in 1980 and added otherwise-eligible women as they because postmenopausal after 1980. Thus, a total of 80,375 women were included in the analysis.
Breast cancer case identification
Diagnoses of breast cancer were ascertained from self-reports on the questionnaire, and medical and pathology records were obtained after the participant or next of kin gave permission. Only invasive breast cancer cases were included. Confirmation of estrogen receptor and progesterone receptor status was obtained by reviewing pathology reports. Deaths were reported by family members or the postal service or were identified from a search of the National Death Index. Ascertainment of deaths in this cohort is estimated to be 98 percent complete (16).
Dietary assessment
The FFQs used to assess diet have been described in detail elsewhere and were completed in 1980, 1984, 1986, 1990, 1994, and 1998 (17, 18). Each food was assigned a common portion size, such as one apple; women were asked how often they had consumed each food on average over the past year, with answers ranging from "never consumed" to "six or more times per day." Nutrient intakes were calculated as described elsewhere (17) and were energy-adjusted using the multivariate nutrient density method (18). The validity of specific fatty acid intakes assessed by FFQ has been previously assessed by comparison with concentrations in subcutaneous fat aspirates: Spearman correlation coefficients were 0.51 for trans-unsaturated fat and 0.48 for long-chain omega-3 fatty acids (19). In addition, correlations comparing the expanded FFQ with multiple 1-week weighed diet records were 0.67 for total fat, 0.70 for saturated fat, 0.64 for polyunsaturated fat, and 0.69 for monounsaturated fat (20). Furthermore, the validity of total fat intake determined from the expanded FFQ used in this analysis has been evaluated using blood triglyceride levels (21).
Statistical methods
Each participant accrued person-years of follow-up starting from the return date of the 1980 questionnaire or the return date of the questionnaire on which she reported becoming postmenopausal, whichever came first. Follow-up continued until the date of breast cancer diagnosis, death, or June 1, 2000. Dietary variation over time was accounted for by calculating the cumulative average intake of nutrients from all available prospectively completed dietary questionnaires. For example, the 1980 diet was related to breast cancer incidence between 1980 and 1984, the average of the 1980 and 1984 diets was related to breast cancer incidence between 1984 and 1986, and so forth.
In additional analyses, we examined latency using the multiple questionnaires to maximize power. For example, for latency of 0–4 years, we used the 1980 questionnaire for cases diagnosed from 1980 to 1984, the 1984 questionnaire for cases diagnosed from 1984 to 1986, the 1986 questionnaire for cases diagnosed from 1986 to 1990, the 1990 questionnaire for cases diagnosed from 1990 to 1994, the 1994 questionnaire for cases diagnosed from 1994 to 1998, and the 1998 questionnaire for cases diagnosed from 1998 to 2000. For latency of 4–8 years, we used the 1980 questionnaire for cases diagnosed from 1984 to 1988, the 1984 question for cases diagnosed from 1988 to 1990, the 1986 questionnaire for cases diagnosed from 1990 to 1994, and so on. The latency analyses were used to examine whether there is a possible lag between dietary fat intake and increased risk of breast cancer.
Substitution models were utilized to represent the replacement of energy from fat with an equal amount of energy from carbohydrate by concurrently including total energy, protein, and fat in the model (22). Furthermore, diet before menopause was used to predict postmenopausal breast cancer risk by using cumulatively averaged diets that were no longer updated once the women became menopausal. Nondietary covariates such as menopausal status, postmenopausal hormone therapy, and body mass index were updated every 2 years on the basis of the returned questionnaires. Covariates were chosen for inclusion in the multivariate model if they were known to be risk factors on the basis of previous research, including the Nurses' Health Study (6). Cox proportional hazards models were used to calculate breast cancer risk adjusted for known risk factors. The p value for linear trend was calculated using a 5 percent increment of energy from fat intake.
Correction for error in the measurement of fat intake by the FFQ was carried out with %BLIN, a SAS macro described elsewhere in detail (23–25), using calibration data obtained from weighed dietary records completed by Nurses' Health Study participants (26). The 1980 validation study was used to correct the relative risk for the first 4 years of follow-up and the 1986 validation study was used to correct for the remaining years of follow-up, because an expanded FFQ was distributed in 1986 and in subsequent years. The data from both analyses were then pooled to obtain the measurement-error correction results for the 20 years of follow-up.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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We documented 3,537 incident cases of invasive breast cancer among 80,375 postmenopausal women between 1980 and 2000. In the age-adjusted analysis, we observed no association between total fat intake and breast cancer risk using the cumulatively averaged and updated percentage of energy derived from total fat (table 1), and results were minimally changed in the multivariate analysis. We also observed no evidence of a decreased risk with very low intake of fat. Using a reference category of 30.1–35 percent of energy derived from fat, the multivariate relative risk of breast cancer associated with a fat intake of
20 percent of energy derived from fat was 1.09 (95 percent CI: 0.72, 1.66). The overall trend was nearly significantly inverse (p-trend = 0.11). No apparent association was seen for any of the four cross-classified categories of estrogen and progesterone receptor status (table 2).
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In analyses using dietary intakes as continuous variables, higher intakes of energy, total fat, animal fat, vegetable fat, polyunsaturated fat, monounsaturated fat, trans-unsaturated fat, long-chain omega-3 fatty acids, cholesterol, and linolenic acid were not associated with increased breast cancer incidence, with or without additional adjustment for other types of fat (table 3). Substitution of carbohydrate with an equal percentage of calories from fat was not associated with an increased risk of breast cancer; for an increment of 5 percent of energy derived from total fat intake, the multivariable relative risk was 0.98 (95 percent CI: 0.95, 1.00). Results for different types of fat were also similar for cancers classified by estrogen and progesterone receptor status. In addition, no significant association with intake of total fat, used as a continuous variable, was observed after adjustments for additional covariates, including vitamin A, vitamin E, and calcium; the multivariable relative risk for an increment of 5 percent of energy from total fat was 0.97 (95 percent CI: 0.94, 1.00). The results including only women who underwent mammography before 1998 were similar; the multivariable relative risk for an increment of 5 percent of energy from total fat was 0.98 (95 percent CI: 0.95, 1.02).
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A significant inverse association between total fat intake and risk of breast cancer was seen among women with waist circumferences equal to or greater than 35 inches (
88.9 cm) (p-trend = 0.04) (table 4). However, in all three strata of body mass index, no significant association was observed between percentage of energy derived from fat and breast cancer risk (table 5).
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We also used the repeated questionnaires to assess the temporal relation between dietary fat intake and breast cancer risk (table 6). No significant association was observed with different latency intervals.
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We also did not observe an association between premenopausal intake of total dietary fat and postmenopausal breast cancer incidence (17,362 women were included in this analysis, with 497 cases); for an increment of 5 percent of energy derived from total fat intake, the relative risk was 1.03 (95 percent CI: 0.96, 1.10) (table 7). Furthermore, premenopausal intakes of specific types of dietary fat were not associated with postmenopausal breast cancer incidence. The one exception was a positive association between trans-unsaturated fat intake and postmenopausal breast cancer risk; the relative risk for an increment of 1 percent of energy was 1.08 (95 percent CI: 1.01, 1.15).
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Additionally, analyses stratified by age of entry indicated no apparent differences in the association between dietary fat and breast cancer risk. The multivariate relative risks for an increment of 5 percent of energy derived from total fat intake were 0.96 (95 percent CI: 0.87, 1.06) for age
40 years, 0.98 (95 percent CI: 0.94, 1.02) for age 40.1–50 years, and 0.98 (95 percent CI: 0.95, 1.02) for age >50 years.
The associations between animal fat intake and breast cancer risk were examined separately for the time periods 1980–1990 and 1990–2000 to replicate the time period of the previous Nurses' Health Study II, in which an association was seen (15). In the 1980–1990 analysis using the cumulative average intake of animal fat from the 1980, 1984, and 1986 dietary questionnaires, the relative risk for an increment of 5 percent of energy was 0.99 (95 percent CI: 0.96, 1.02). In the 1990–2000 analysis using the 1990, 1994, and 1998 questionnaires, the relative risk was 1.01 (95 percent CI: 0.97, 1.04).
An analysis correcting for error in measurement of fat intake was conducted with fat intake measured as a continuous variable. The uncorrected relative risk for an increment of 5 percent of energy from total fat was 0.98 (95 percent CI: 0.95, 1.01). In comparison, the relative risk corrected for measurement error was 0.96 (95 percent CI: 0.91, 1.02).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Our study provides further evidence that higher dietary fat intake during mid- and later life does not appreciably increase breast cancer risk. Specific types of dietary fat were also not significantly associated with risk of breast cancer. Our results are consistent with a large body of prospective studies with shorter follow-up periods (6
). The possible positive association between total fat intake and breast cancer risk observed in a recent meta-analysis may be attributed to biases in case-control studies, because an increased risk was observed only in these studies (27). In addition, the recent meta-analysis suggested an increased risk for breast cancer with greater intakes of saturated fat and meat in both case-control and cohort studies (28). However, the pooled analysis of eight cohort studies indicated no significant increase in breast cancer risk with greater intake of meat or saturated fat (5). The pooled analysis represents a superior method, because the analysis was conducted using raw data rather than combining published risk estimates, which allows a consistent analytical approach in all studies and is less susceptible to publication bias. In addition, previous analysis from the Nurses' Health Study indicated no significant association between meat intake and breast cancer risk (29).
Unlike the recent report from the Women's Health Initiative (14), we found no evidence that the association between dietary fat and breast cancer risk differed by the estrogen or progesterone status of the tumor. The significant elevation in risk in the lowest fat-intake group for the estrogen receptor-positive/progesterone receptor-negative cancers in our study suggests that a low-fat diet is unlikely to reduce risk of this subset of cancers and that the finding from the post hoc analysis in the Women's Health Initiative is most likely due to chance.
The significantly lower risk of breast cancer with higher total fat intake among women with greater waist circumferences may be explained by the exaggerated adverse metabolic effects of high-carbohydrate/low-fat diets, including hyperinsulinemia, among persons with greater insulin resistance (21, 30). Hyperinsulinemia has been hypothesized to increase breast cancer risk by reducing the production of sex hormone-binding globulin, which increases the level of free estrogen, as well as by inhibiting apoptosis (31, 32). Waist circumference may be a better indicator of insulin resistance than body mass index (33), because results for stratification by body mass index were not significant.
A limitation of this study is that we were unable to investigate diets with less than 15 percent of calories derived from fat. In addition, this study does not address the effect of diet during childhood and early adult life. This study, like all studies, could be subject to unmeasured confounding. However, the difficulties demonstrated by the Women's Health Initiative show that a definitive randomized trial may never be carried out. Despite a goal of 20 percent of energy derived from fat in the intervention group and 40 percent of energy derived from fat in the control group, the actual difference between the intervention group and the control group as reported by participants at the study's end was 8.1 percent of energy, a difference that would make a true effect difficult to observe. In addition, serum levels of high density lipoprotein cholesterol and triglycerides, which are influenced by the percentage of calories derived from fat in the diet, differed little between the intervention and control groups. This suggests that the actual difference in fat intake between the two groups may have been even smaller than reported (14), which would be consistent with the finding that participants in intervention studies generally overstate their compliance in comparison with biochemical indicators. Even if a small effect were to emerge with continued follow-up of the Women's Health Initiative participants, it would be difficult to know whether this was due to a reduction in dietary fat or to the small increase in fruit consumption or the decrease in weight that was seen in the intervention group.
Concern has been raised that error in the measurement of dietary fat could obscure a positive association with breast cancer (34, 35). In a small study recently conducted in England (35) (n = 168 breast cancer cases), a strong positive association between saturated fat intake assessed by diet record and breast cancer incidence was reported, but a weaker association was described for saturated fat intake assessed by FFQ. The authors attributed the difference in findings to greater measurement error by a single FFQ. However, they adjusted the food frequency data for total energy but did not do so for the diet record data. The results for both total fat and saturated fat assessed by the two methods were not likely to have been significantly different, as the confidence interval for the top category of intake with the diary method readily included the relative risk found with the FFQ (35). Furthermore, correction of our findings for measurement error did not significantly change the point estimate; it merely produced slighter larger confidence intervals.
This study has many strengths, since to our knowledge it is one of the largest and longest prospective studies of dietary fat and breast cancer risk carried out to date. The 20 years of follow-up and repeated measures of diet allowed investigation of a wide range of latencies between dietary fat intake and diagnosis of breast cancer. Furthermore, we were able to adjust for many potential confounders, stratify by waist circumference and body mass index, and restrict the analysis to women who had undergone mammographic screening. In our study, the use of repeated questionnaires substantially reduced the measurement error in assessment of long-term fat intake; for example, for total fat, the correlation between the average of three FFQs and the mean of the 1980 and 1986 diet records was 0.83 (36). In addition, total fat intake assessed by our questionnaire had predicted levels of fasting triglyceride, as expected by controlled feeding studies (21). Moreover, in this same cohort (but with fewer cases), intakes of specific types of fat have predicted incidence of coronary heart disease (37) and type 2 diabetes (38), as would be expected from their metabolic effects. Furthermore, the large number of incident cases and resulting narrow confidence intervals, with an upper bound of 1.00 for total fat, ensures that an important positive association is unlikely to have been missed.
There are major differences in the characteristics of the participants in the present analyses as compared with the previous Nurses' Health Study II analysis, in which we observed a significant increase in breast cancer risk with increasing intake of animal fat, mainly due to high-fat dairy products. The present study was based on the original Nurses' Health Study, which included women aged 34–59 years at the start of follow-up, as compared with 27–44 years in Nurses' Health Study II. In addition, only postmenopausal women were examined in this analysis, whereas in the Nurses' Health Study II analysis all of the women were premenopausal at baseline. Thus, the differences in findings for animal fat might be explained by the different susceptibility of breast tissue during the early reproductive years. However, it seems unlikely that differences in findings are due to recent changes in food production or processing, because our findings for animal fat intake and breast cancer were similar for the periods 1980–1990 and 1990–2000.
Although we did not find any relation between dietary total fat during the premenopausal years and risk of breast cancer after menopause, the youngest women were 34 years of age in 1980; thus, an effect of diet earlier in adulthood may have been missed. However, the small increase in risk of postmenopausal breast cancer with higher premenopausal intakes of trans-unsaturated fats should be addressed in future studies.
In summary, this 20-year prospective follow-up of our large cohort does not support the hypothesis of a positive association between intake of total or specific types of dietary fat and risk of postmenopausal breast cancer. Limiting total dietary fat or specific types of dietary fat during midlife and the postmenopausal years is unlikely to be an effective means of preventing breast cancer.
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ACKNOWLEDGMENTS |
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This work was supported by National Institutes of Health grant CA87969.
The authors acknowledge the invaluable programming assistance of Ya Hua Chen, Ellen Hertzmark, and Dr. Donna Spiegelman.
Conflict of interest: none declared.
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