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© 2007 The American Society for Nutrition J. Nutr. 137:170S-174S, January 2007

Supplement: International Research Conference on Food, Nutrition, and Cancer

Changes in Dietary Fat and Fiber and Serum Hormone Concentrations: Nutritional Strategies for Breast Cancer Prevention over the Life Course1–3,

Michele R. Forman*

Department of Epidemiology, MD Anderson Cancer Center, Houston, TX

* To whom correspondence should be addressed. E-mail: mforman{at}mdanderson.org.


   ABSTRACT
TOP
 ABSTRACT
Introduction
 Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 
The association between dietary fat intake and breast cancer risk has appeared in a meta-analysis of epidemiologic research, migration studies from countries of low to high risk for breast cancer, and animal experiments. With this background, dietary intervention research aims to reduce fat intake and increase fruit, vegetable, and fiber intake, relying on changes in hormone concentrations as biomarkers for reduction in risk of breast cancer. To date, this dietary intervention research spans the life course and has demonstrated stellar success in some studies but sobering results in others. The purpose of this article is to review the intervention research since a 1999 meta-analysis that reported reduced estradiol levels on a low-fat diet and to explore the lessons learned from intervention research on changes in dietary fat and fiber intake and serum hormone concentrations. Secular trends in obesity and ages at pubertal onset and menarche provide dynamic behavioral, genetic, and developmental challenges to the success of dietary prevention. The goal is to formulate an integrative approach to dietary intervention, taking into consideration ethnic group differences in energy expenditure that modulate weight and hormones influencing breast cancer risk over the life course.


   Introduction
TOP
 ABSTRACT
 Introduction
Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 
The association between dietary fat intake and risk of breast cancer has been examined in ecological, etiologic, and intervention research and animal experiments. In a country-by-country ecological comparison, increasing fat intake (from national food balance data) was directly related to breast cancer incidence and mortality as the socioeconomic status of the country improved (1–3). Ecological data provided the backdrop to the etiologic epidemiology studies. For example, Iranian women who migrated from their low-risk country of origin experienced 4-fold higher breast cancer rates in the same generation of immigrants to Canada (4). In a meta-analysis of epidemiologic research on total fat intake and breast cancer risk, the summary estimates of the odds ratio of breast cancer from case-control studies and risk from cohort studies were 1.14 (95% CI 0.99, 1.32) and 1.11 (95% CI 0.99, 1.25), respectively, among women who consumed the highest vs. lowest fat intake (5). Also, evidence from animal research documented a lower rate of mammary tumors and metastases in rodents placed on diets of <20% energy from fat compared with the AIN control diet group (6–8). These results appeared in nonovariectomized and ovariectomized rodents and with the administration of tamoxifen (i.e., selective estrogen modulators) (8).

The association between fiber intake and breast cancer has a more limited portfolio of research than the association between fat intake and breast cancer. A consistent inverse association between dietary fiber intake (from whole grains and raw vegetables) and breast cancer has been reported in case-control but not cohort studies (9). Dietary fat promotes intestinal reabsorption of estrogens by enhancement of deconjugating enzyme activity, whereas intraluminal fiber retards the process. Further evidence appears in research comparing vegetarians with omnivores, wherein urinary estrogen levels are higher in omnivores than vegetarians, and, conversely, fecal estrogens are higher in vegetarians than omnivores. Also, breast cancer incidence rates are lower in lifelong vegetarians than in omnivores (10).

The effect of low-fat, high-fiber diets on serum estradiol (E2)4 concentrations was summarized in a meta-analysis of 15 dietary intervention studies in 1999 (11). There was a 13% reduction in E2 levels overall; however, study designs, percentage reduction in fat and increase in fiber intakes, and hormonal effects differed by menopausal status. Specifically, in the meta-analysis of 6 controlled feeding studies over 1 to 2 menstrual cycles and 1 randomized trial or 3 counseling studies in the free-living state (duration 15–112 wk) in premenopausal women, a summary estimate of a 7% decline in E2 levels while on diet was reported. In the meta-analysis of 5 dietary counseling studies with lists of proscribed foods and foods to limit intake over 3–20 wk in postmenopausal women, a 23% decline in E2 levels overall was reported. The larger percentage decline in postmenopausal than premenopausal women is offset by the smaller and lower range in E2 levels in the former group. Since 1999, several intervention studies were reported in healthy women and girls over the life course, yet no review has been conducted. Over the same time, secular trends in obesity and age at onset of puberty and menarche differed by ethnic group; these trends have implications for future research. In this article we review the low-fat, high-fiber intervention research since 1998, examine the lessons learned from successes and those studies that were not so successful, and thread the review with observational studies that have implications for future research in diet and breast cancer. The approach is taken from the life-course paradigm to examine opportunities for prevention in the context of findings from observational research to identify the high risk and tailor applications.


   Materials and Methods
TOP
 ABSTRACT
 Introduction
 Materials and Methods
Results
 Discussion
 LITERATURE CITED
 
A search for published dietary intervention studies on the effect of dietary fat and fiber intakes and serum hormone concentrations in women was conducted using PubMed, Clinical Trials.gov, and biomed central from 1990 to the present. The terms for the search included dietary intervention or prevention; hormone concentrations; intake of fat and of fiber; premenopausal and postmenopausal women, girls; and breast cancer. The research was limited to women who had not been diagnosed with breast cancer. Because limited information on physical activity was provided in the articles, no data are presented even though physical activity is an integral component of energy balance and influences hormone levels. Physical activity and other aspects of energy balance are addressed in the Discussion.


   Results
TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
Discussion
 LITERATURE CITED
 
    Observational data on prenatal growth and puberty. Compared with appropriate-for-gestational-age (AGA: 10th–90th percentile for gender-specific birth weight for gestation age) children, those small for gestational age (SGA: <10th percentile of gender-specific birth weight for gestation age) experienced catch-up (or -down) growth by age 2 y (12). SGA girls with catch-up growth experienced puberty and menarche ~5–10 mo earlier than those without catch-up growth and AGA girls. A monotonic relation was noted between the increasing delay in the age at menarche in girls who have precocious puberty and birthweight-for-gestational-age ranges from the extreme SGA through AGA (12). However, SGA girls have a smaller uterus and ovaries than do AGA girls in late adolescence (12).

    Ethnic-group difference in puberty and menarche. In the United States the trend in the mean or median ages of entry into puberty (i.e., Tanner breast stage 2) differed by ethnic group (13). The age of pubertal onset in non-Hispanic white girls declined from the 1940s through the 1990s. A sharper decline in the age of pubertal onset in African American girls occurred from the 1960s through the 1990s. In non-Hispanic white and African American girls, the age at onset of puberty stabilized relatively recently at 10.2 and 9.8 y, respectively; and similar findings appeared in snapshots from cross-sectional national surveys and in longitudinal prospective cohort studies (13–18). Specifically, 615 non-Hispanic white girls and 541 African American girls aged 9 y were recruited from 3 regions of the country for a longitudinal study, the National Heart, Lung, and Blood Institute Growth and Heath Study (NGHS). The population was socioeconomically diverse, and data reflected ethnic group differences in the age at onset of puberty. African American girls experienced the onset and completion of puberty at 9.6 y (95% CI 9.5, 9.7) and 13.6 y (95% CI 13.5, 13.6) in contrast with non-Hispanic whites, who experienced the same developmental hurdles at 10.2 y (95% CI 10.2, 10.3) and 14.3 y (95% CI 14.2, 14.4), respectively (14). The NGHS girls and those participating in the National Health and Nutrition Examination Surveys 1988–1994 were the same birth cohorts; thus, the comparability in findings and birth cohorts supported ethnic-group trends in puberty.

The distinctions intensify in a study of the distribution of cytochrome P450 3A4*1 genotypes in girls aged 9.5 y by ethnicity and by pubertal stage (19). CYP 3A4 is an isoenzyme on the steroid hormone cascade responsible for metabolizing T to 2-, 6-, and 16-ß dehydroxytestosterone. About 62% of the African American girls, 52% of the Hispanic white girls, and 17% of the non-Hispanic white girls had the 1B/*1B allele. Most interestingly, 90% of the girls who had the 1B/*1B allele were classified as pubertal (i.e., ≥Tanner stage B2) by pediatricians after adjustment for BMI, age, and ethnicity compared with 40% of girls who had the 1A/1A allele.

In the United States the average age at menarche also differed by ethnicity over time. On average, non-Hispanic white girls were 12.9 y when they had their first menses in the 1940s; the age declined to 12.8 y in the 1960s and to 12.57 and 12.52 y in the early and late 1990s, respectively. African American girls were 12.5 y when they had their first menses in the 1960s, and the age declined to 12.09 and 12.06 y in the early and late 1990s, respectively. Finally, Mexican American girls experienced a decline in the average age at menarche from 12.24 y in the 1980s to 12.09 y in the late 1990s (20). The above mentioned secular trends in puberty and menarche were reported concurrently with findings from or the conduct of dietary intervention research presented below.

    Dietary intervention studies across the life course. In the Dietary Intervention Study in Children, 286 healthy, prepubertal girls with elevated low-density lipoprotein cholesterol levels (≥80th percentile for age) were randomly assigned to their usual diet or a behavioral intervention aimed at reducing dietary fat from 33% to 27% of energy per day for 7 y. Over 90% of the girls were non-Hispanic white. All girls were postmenarchal at the end of the trial. By year 5, the girls on the intervention diet had significantly lower serum estrone, estrone sulfate, and E2 levels by 21–30% compared with girls on their usual diet. By the last year, serum progesterone levels were 53% lower in the intervention than the control group, but no significant differences appeared in E2 or its metabolites (21).

Wong et al. (22–24) conducted a metabolic ward study of 147 girls aged 8–17 y to compare energy expenditure, serum hormone levels, and anthropometry in African Americans and non-Hispanic whites. Energy expenditure was measured by whole-room indirect calorimetry and in free-living conditions by the doubly labeled water method. After adjustment for Tanner stage, age, energy intake, and fat mass, mean energy expenditure was significantly lower in sleeping, basal, and free-living states and during physical activity in African American girls compared with non-Hispanic white girls. Yet, mean height, BMI, and free insulin-like growth factor-1 (IGF-1) and leptin levels were significantly higher in African American than non-Hispanic white girls. Ethnic-group differences in energy expenditure appeared in most but not all prior research (25), whereas ethnic group differences in hormonal and anthropometric status were more consistent (13,14).

    Observational data on the cyclic fluctuation of hormones by ethnicity. In the largest study to date, including over 1000 women, Haiman et al. (26) described the cyclic fluctuation of hormones and percentage of anovulatory cycles by ethnicity. Compared with African American women, Latina and non-Hispanic white women, respectively, had 9.9% and 17.4% lower E2 levels in the follicular phase and 9.4% and 25.3% lower E2 levels in the luteal phase. Serum progesterone levels were 15.4% and 36.4% lower in Latina and non-Hispanic white women, respectively, than African American women in the luteal phase. Moreover, 7% of the African American and Latina women experienced anovulatory cycles in contrast with 14% of non-Hispanic white women. Ethnic group differences were larger when the analysis was restricted to women of normal BMI who had ≤3000 metabolic equivalents-min/wk. Similar endogenous hormonal differences in African American and Caucasian women appeared in the Nurses' Health Study II (27). Knowledge of ethnic group differences in hormonal fluctuations is essential for sample selection and calculation of expected changes in serum hormone concentrations in future intervention research in premenopausal women.

    Controlled dietary research in premenopausal women. Ethnic-group differences in serum hormone levels were reported in an earlier low-fat, high-fiber controlled feeding study (28). At baseline, serum E2, free E2, estrone, and androstenedione levels were significantly lower in non-Hispanic white than African American women. After 21 d on a diet of lower fat (reduced by 20%) and higher fiber (increased from 12 to 40 g/d), E2 concentrations were lower by 8.5% in the African American women and by 37% in non-Hispanic white women, whereas free E2 levels were reduced by 30% in the latter group only. Moreover, serum androstenedione levels were 48% lower in non-Hispanic white women but 18% higher in African American women, indicating further differential effects of the dietary plan on hormone levels by ethnicity. No other published data have reported ethnic-group differences from a low-fat, high-fiber plan under controlled dietary conditions.

    Diet and hormone study. In the free-living state, 213 healthy, premenopausal women aged 20–40 y were randomly assigned to remain on their usual diet or to consume a low-fat, high-fiber diet of <20% energy from fat, 25–30 g/d of fiber, and >8 daily servings of fruit and vegetables for 1 y (29). Anthropometry measurements were taken, dietary intakes were reported in a food frequency questionnaire and three 24-h recalls, and blood samples were collected at baseline and at the 4th and 12th menstrual cycles. The women were instructed to use OvuQuick to determine date of ovulation and date for a blood collection during the midluteal phase of the cycle. Women were not encouraged to reduce energy intake or weight during the study; most participants were non-Hispanic whites. From baseline to the 12th cycle, the intervention group had significantly reduced fat intake by 31 g/d and increased fiber intake to 36%; their serum E2 and free E2 levels were 7–8% lower than those in the control group.

    Diet and androgens trial. Postmenopausal women in the highest tertile of T levels (n = 312) were randomly assigned to a diet low in animal fat and refined carbohydrate and rich in low-glycemic-index foods, mono- and (n-3) polyunsaturated fatty acids, and phytoestrogens or to their usual diet for 18 wk (30). The intervention group experienced an intensive 18 wk of meals and cooking classes with daily consumption of whole wheat and flaxseed bread, a Mediterranean diet, and soy, while meat, eggs, and dairy intakes were reduced to once per week. The control and intervention groups provided 10 and 24 24-h food frequency questionnaires, respectively, over the course of the trial. After adjustment for weight change and age, serum sex-hormone binding globulin levels had increased by 25% vs. 4% in the intervention and control groups, respectively, whereas IGF binding protein (IGFBP)-1 and IGFBP-2 had also increased by 12% and 30%, respectively, in the intervention group in contrast with a 6% decline in IGFBP-1 and a 6% increase in IGFBP-2 in the control group (31). Also, serum T, free T, and free E2 concentrations were significantly lower by 19.5%, 28.6%, and 5.7%, respectively, in the intervention group after the trial. On average, the intervention group lost 4 kg compared with <0.5 kg in the control group over 4.5 mo.

    Women's Health Initiative. Forty percent of Women's Health Initiative (WHI) trial participants were assigned at baseline to the low-fat, high-fruit-and-vegetable arm, whereas the remaining 60% were on their usual diets. The WHI was a 40-center trial of postmenopausal women using a multifactorial design for 10 y in the United States. Prentice et al. (32) recently reported the effect of the low-fat, high-fiber dietary intervention on the incidence of breast cancer. The annualized cumulative hazard for invasive breast cancer was lower in the dietary intervention than the control group, with a hazard ratio of 0.91 (95% CI 0.83, 1.01) over the 8.1-y average follow-up. Larger effects were observed among women who were classified as adhering to the dietary plan than among the overall intervention group. Serum E2 levels after 1 y of the trial were significantly lower by 15% in the intervention group compared with those on their usual diets.


   Discussion
TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
 Discussion
LITERATURE CITED
 
After >20 y of intervention research, several low-fat, high-fiber dietary interventions reduced serum E2 and free E2 levels in girls, premenopausal women, and postmenopausal women, but results were not always statistically significant and specific hormonal changes did not remain over time (21,29). Dietary intervention regimens differed across studies, thereby reducing the opportunity to effectively identify a threshold or a dietary plan that might be applied in larger populations of women or girls. Before 1998, intervention effects on serum E2 levels were routinely reported even though concentrations of estrone and its sulfate were significantly reduced by 16–36% in premenopausal women who participated in 5 of 6 studies in the earlier meta-analysis (11). Since 1998, dietary intervention research has broadened the focus to hormones such as IGF-1, T, and free-T levels in women and girls (21,30). Yet to date, too few intervention studies have been conducted to examine effects on specific hormones other than estrogens by menopausal status. Thus, a conclusion that a low-fat, high-fiber diet modifies serum hormone concentrations, which in turn reduce the risk of breast cancer, is not clear from this review.

Two elements of energy balance, notably weight loss and physical activity, were not routinely reported across intervention studies. In research on postmenopausal women, a dietary plan that reduces fat and enhances fiber intake reduced weight as evidenced in 5 of 6 dietary intervention studies over time (11,30). Under extreme conditions such as anorexia or very low body mass, endogenous hormone concentrations and lifetime risk of breast cancer are lower than in normal-weight women (33,34). Perhaps it is also time to challenge the traditional approach to controlled feeding studies and modify the design to monitor weight change without isocaloric conditions.

To date, a fairly consistent pattern of lower energy expenditure and higher hormone concentrations in African American girls and premenopausal women compared with non-Hispanic white girls and women has appeared, whereas data on energy expenditure in Hispanic whites and Asians have not been published. Future dietary intervention research may require tailoring dietary plans within the context of recognized ethnic group differences in energy expenditure and endogenous hormone levels.

Given the secular trends in obesity and in ages at onset of puberty and menarche as well as ethnic-group differences in energy expenditure, what are the opportunities for breast cancer prevention across the life course? Is energy expenditure set in utero? If so, how does the programming influence prevention research? Free E2 levels vary over the menstrual cycle by level of physical activity in women who differ by body fatness or ponderal index at birth (35). Identification of the intensity of physical activity to reduce breast cancer risk may require an assessment of the woman's nutritional status at birth. Thus, fetal programming of reproductive function (indicated by responsiveness of steroid hormone levels to intensity of physical activity in the reproductive years), dietary intervention, energy expenditure, and weight loss are factors to integrate in a paradigm for breast cancer prevention.

Higher rates of SGA but greater chances of survival within birth weight-for-gestation groups and lower energy expenditure during puberty in African American than non-Hispanic white girls support the possibility that African American girls are born with a lower energy expenditure than non-Hispanic white girls. Similar data are not available for Hispanics and Asians in the United States. Recent data reveal that catch-up growth in the first 2 y of life among those born SGA influences age at puberty and menarche (12,36). Will dietary interventions be tailored for prevention by early-life growth trajectories coupled with physical activity to enhance efficacy? In the United States we need to establish tracking systems for growth over the life course to facilitate accrual of participants by early growth parameters. Should we refine selection of participants in future dietary trials, for example, to gene polymorphisms for LDL-C in African Americans that are suppressed with increasing dietary cholesterol intake to tailor prevention modalities (37)? The role of molecular markers during specific windows of the life course such as the gene polymorphisms in cytochrome P450 that vary by ethnic group and early pubertal development are currently being explored in a larger study of young African American and Mexican American girls. With increasing findings from molecular, behavioral, nutritional, and endocrine sciences, the challenge is how to tailor interventions to delay puberty (and thereby greater cumulative life exposure to hormones) specifically for ethnic groups. At the same time, we need to sharpen our tools for dietary and physical activity assessment to forecast prevention and intervention modalities later in the life course as other windows for modification of hormones and breast cancer risk present themselves.


   FOOTNOTES
 
1 Published in a supplement to The Journal of Nutrition. Presented as part of the International Research Conference on Food, Nutrition, and Cancer held in Washington, DC, July 13–14, 2006. This conference was organized by the American Institute for Cancer Research and the World Cancer Research Fund International and sponsored by (in alphabetical order) the California Walnut Commission; Campbell Soup Company; Cranberry Institute; Hormel Institute; IP-6 International, Inc.; Kyushu University, Japan Graduate School of Agriculture; National Fisheries Institute; and United Soybean Board. Guest editors for this symposium were Vay Liang W. Go, Susan Higginbotham, and Ivana Vucenik. Guest Editor Disclosure: V.L.W. Go, no relationships to disclose; S. Higginbotham and I. Vucenik are employed by the conference sponsor, the American Institute for Cancer Research. Back

2 Author Disclosure: No relationships to disclose. Back

3 This work was funded by the Intramural Program/Center for Cancer Research, National Cancer Institute. The author has no potential conflicts of interest. Back

4Abbreviations used: AGA, appropriate for gestational age; E2, estradiol; IGF-1, insulin-like growth factor-1; IGFBP, IGF binding protein; NGHS, National Heart, Lung, and Blood Institute Growth and Heath Study; SGA, small-for-gestational age; T, testosterone; WHI, Women's Health Initiative. Back


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TOP
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 Introduction
 Materials and Methods
 Results
 Discussion
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