Background: The results of previous studies on diet and postmenopausal breast cancer risk have been inconclusive, but there is some evidence that dietary patterns developed to correlate with estrogen levels are associated with breast cancer. We aimed to examine the association of a previously developed estrogen-related dietary pattern (ERDP) with postmenopausal breast cancer in the Sister Study.

Methods: The ERDP was calculated from food frequency questionnaire responses among Sister Study participants without a personal history of cancer and who contributed postmenopausal person-time at risk. Cox proportional hazards models were used to estimate HRs and 95% confidence intervals for the association between the ERDP and postmenopausal breast cancer.

Results: With more than 261,959 person-years of follow-up and 1,968 incident cases, the ERDP was not associated with total, invasive, estrogen receptor (ER)-positive or ER-negative subtypes of breast cancer. Results were robust to various sensitivity analyses.

Conclusions: The results do not support previous studies observing a positive association between a proestrogenic dietary pattern and postmenopausal breast cancer risk. Null results may be partially explained by high levels of other breast cancer risk factors within the study population, such as a family history of breast cancer.

Impact: An estrogen-related dietary pattern may not be a strong predictor of breast cancer risk in all populations. Future studies of diet and breast cancer should evaluate the potential for effect modification by family history and consider differences in dietary assessment tools when comparing results across study populations. Cancer Epidemiol Biomarkers Prev; 27(10); 1223–6. ©2018 AACR.

Estrogen is an established risk factor for postmenopausal breast cancer and has been suggested to partially mediate associations between lifestyle factors such as adiposity and breast cancer (1). Dietary factors can influence estrogen metabolism (2); however, studies of diet and breast cancer have been inconclusive. Dietary patterns developed to reflect estrogen exposure have been associated with breast cancer in some populations (3, 4), but not all (5). One such pattern, the estrogen-related dietary pattern (ERDP; ref. 4), was developed in the Prostate, Lung, Colorectal and Ovarian Cancer (PLCO) Screening Trial to identify food groups that explained the largest variation in levels of unconjugated estradiol and the ratio of 2- and 16-hydroxylated estrogen metabolites, which have been associated with breast cancer risk (6). The ERDP was positively associated with total, invasive, and estrogen receptor (ER)-positive postmenopausal breast cancer in the PLCO (4). We aimed to examine the generalizability of the ERDP by examining its association with total, invasive, and ER subtypes of breast cancer in a separate study of postmenopausal women.

The Sister Study, described elsewhere (7), is a prospective cohort of 50,884 women ages 35 to 74 years recruited between 2003 and 2009, all with a sister who was diagnosed with breast cancer, followed up through August 2015 (data release 5.0.1). In the current analysis, participants were excluded if they had a personal history of cancer (n = 2,757), did not contribute any postmenopausal person-time at risk (n = 8,014), reported an extreme caloric intake (<500 or >5,000 kcal/day; n = 1,162), had an extreme body mass index (BMI; <15 or >50 kg/m2; n = 68), or had missing covariate data (n = 958), bringing the analytic sample to 37,925.

Scoring of the ERDP has been described elsewhere (4). Briefly, the ERDP was calculated by summing across the weighted intakes of 11 previously identified food groups (shown in Table 1) using usual intakes over the past 12 months as measured by a 110 item block food frequency questionnaire (FFQ). Breast cancer cases were ascertained via self-report and confirmed with medical records. Because the positive predictive value of self-reported breast cancer was 99%, self-reports were used when records were not available.

Table 1.

Population characteristics across quartiles of the ERDP score, Sister Study, 2003–2009

ERDP quartile (score range)
1st2nd3rd4th
(−8.2344 to −0.4442)(−0.4441 to −0.0584)(−0.0583 to 0.3467)(0.3468 to 4.6661)
n 9,481 9,482 9,481 9,481 
Breast cancer cases Total 520 474 484 490 
 Invasive 393 368 350 373 
 Invasive ER+ 308 268 250 272 
 Invasive ER 47 46 52 56 
ERDP score (mean ± SD) −0.90 ± 0.48 −0.24 ± 0.11 0.13 ± 0.12 0.82 ± 0.47 
Age (mean ± SD) 58.3 ± 7.3 58.1 ± 7.5 57.2 ± 7.8 56.0 ± 7.6 
BMI (kg/m2; mean ± SD) 27.0 ± 5.5 27.4 ± 5.6 28.0 ± 6.0 28.7 ± 6.6 
BMI at age 30 (kg/m2; mean ± SD) 22.7 ± 3.3 22.7 ± 3.3 23.0 ± 3.5 23.4 ± 4.0 
Total caloric intake (kcal/day) 1,601 ± 590 1,439 ± 532 1,527 ± 535 1,908 ± 649 
MET-hours/week (mean ± SD) 53.4 ± 31.9 51.1 ± 31.0 49.6 ± 30.9 49.8 ± 31.1 
Age at menarche (mean ± SD) 12.6 ± 1.5 12.6 ± 1.5 12.6 ± 1.5 12.7 ± 1.6 
Age at menopause (mean ± SD) 50.3 ± 5.8 50.1 ± 5.9 49.9 ± 6.1 49.8 ± 5.9 
Number of relatives with family history (mean ± SD) 1.27 ± 0.59 1.28 ± 0.59 1.27 ± 0.58 1.26 ± 0.57 
Parity (mean ± SD) 1.95 ± 1.35 2.01 ± 1.35 2.02 ± 1.37 1.96 ± 1.37 
Nulliparous (%) 18.2 16.6 17.2 18.6 
PHT status (%)     
 Never 44.6 45.8  48.1 52.0 
 Former: estrogen + progesterone 24.4 22.7 21.7 19.4 
 Former: estrogen only 16.8 17.1 15.7 14.8 
 Former: unknown what type 2.3 2.3 2.4 2.4 
 Current: estrogen + progesterone 5.2 5.0 5.1 4.6 
 Current: estrogen only 6.7 7.1  7.0  6.8 
Race/ethnicity (%)     
 White, non-Hispanic 85.6 84.7 85.0 86.4 
 Black, non-Hispanic 8.3 8.1 7.9 5.5 
 Hispanic 2.8 4.3 4.5 5.2 
 Asian 0.9 0.7 0.5 0.3 
 Other 2.4 2.2 2.1 2.6 
Alcohol (%)     
 Abstainer 17.8 18.6 19.9 21.1 
 ≤1 drink/day 70.7 69.8 69.5 67.0 
 >1 drink/day 11.5 11.6 10.6 11.9 
Smoking (%)     
 Current 7.9 7.8 7.5 8.1 
 Former 41.8 38.5 35.0 35.1 
 Never 50.3 53.7 57.5 56.8 
Education (%)     
 <HS 0.9 1.1 1.2 1.2 
 HS grad or some college 32.4 35.0 36.2 34.8 
 College grad 39.6 39.0 39.7 41.3 
 Postgraduate 27.1 24.9 22.9 22.7 
Hysterectomy (%)     
 No 65.6 65.5 65.0 66.8 
 Yes 34.4 34.5 35.0 33.2 
Non-whole/refined grains (oz/day; mean ± SD) 2.32 ± 1.26 2.39 ± 1.23 2.82 ± 1.34 3.94 ± 1.98 
Tomatoes (cups/day; mean ± SD) 0.24 ± 0.17 0.23 ± 0.17 0.25 ± 0.19 0.35 ± 0.28 
Other vegetables (cups/day; mean ± SD) 0.63 ± 0.51 0.44 ± 0.33 0.40 ± 0.29 0.45 ± 0.31 
Cruciferous vegetables (cups/day; mean ± SD) 0.23 ± 0.27 0.20 ± 0.24 0.22 ± 0.25 0.29 ± 0.41 
Cheese (cups/day; mean ± SD) 0.26 ± 0.21 0.28 ± 0.21 0.36 ± 0.24 0.66 ± 0.41 
Yogurt (cups/day; mean ± SD) 0.23 ± 0.28 0.10 ± 0.14 0.08 ± 0.12 0.06 ± 0.11 
Fish/shellfish high in ω-3 fatty acids (oz/day; mean ± SD) 0.18 ± 0.23 0.14 ± 0.17 0.13 ± 0.17 0.15 ± 0.22 
Fish/shellfish low in ω-3 fatty acids (oz/day; mean ± SD) 0.58 ± 0.63 0.40 ± 0.36 0.38 ± 0.34 0.42 ± 0.41 
Franks and luncheon meats (oz/day; mean ± SD) 0.37 ± 0.32 0.41 ± 0.33 0.51 ± 0.37 0.78 ± 0.59 
Nuts and seeds (oz/day; mean ± SD) 2.11 ± 2.26 1.31 ± 1.33 1.14 ± 1.17 1.20 ± 1.20 
Coffee (cups/day; mean ± SD) 2.19 ± 1.68 1.58 ± 1.40 1.19 ± 1.28 1.02 ± 1.25 
ERDP quartile (score range)
1st2nd3rd4th
(−8.2344 to −0.4442)(−0.4441 to −0.0584)(−0.0583 to 0.3467)(0.3468 to 4.6661)
n 9,481 9,482 9,481 9,481 
Breast cancer cases Total 520 474 484 490 
 Invasive 393 368 350 373 
 Invasive ER+ 308 268 250 272 
 Invasive ER 47 46 52 56 
ERDP score (mean ± SD) −0.90 ± 0.48 −0.24 ± 0.11 0.13 ± 0.12 0.82 ± 0.47 
Age (mean ± SD) 58.3 ± 7.3 58.1 ± 7.5 57.2 ± 7.8 56.0 ± 7.6 
BMI (kg/m2; mean ± SD) 27.0 ± 5.5 27.4 ± 5.6 28.0 ± 6.0 28.7 ± 6.6 
BMI at age 30 (kg/m2; mean ± SD) 22.7 ± 3.3 22.7 ± 3.3 23.0 ± 3.5 23.4 ± 4.0 
Total caloric intake (kcal/day) 1,601 ± 590 1,439 ± 532 1,527 ± 535 1,908 ± 649 
MET-hours/week (mean ± SD) 53.4 ± 31.9 51.1 ± 31.0 49.6 ± 30.9 49.8 ± 31.1 
Age at menarche (mean ± SD) 12.6 ± 1.5 12.6 ± 1.5 12.6 ± 1.5 12.7 ± 1.6 
Age at menopause (mean ± SD) 50.3 ± 5.8 50.1 ± 5.9 49.9 ± 6.1 49.8 ± 5.9 
Number of relatives with family history (mean ± SD) 1.27 ± 0.59 1.28 ± 0.59 1.27 ± 0.58 1.26 ± 0.57 
Parity (mean ± SD) 1.95 ± 1.35 2.01 ± 1.35 2.02 ± 1.37 1.96 ± 1.37 
Nulliparous (%) 18.2 16.6 17.2 18.6 
PHT status (%)     
 Never 44.6 45.8  48.1 52.0 
 Former: estrogen + progesterone 24.4 22.7 21.7 19.4 
 Former: estrogen only 16.8 17.1 15.7 14.8 
 Former: unknown what type 2.3 2.3 2.4 2.4 
 Current: estrogen + progesterone 5.2 5.0 5.1 4.6 
 Current: estrogen only 6.7 7.1  7.0  6.8 
Race/ethnicity (%)     
 White, non-Hispanic 85.6 84.7 85.0 86.4 
 Black, non-Hispanic 8.3 8.1 7.9 5.5 
 Hispanic 2.8 4.3 4.5 5.2 
 Asian 0.9 0.7 0.5 0.3 
 Other 2.4 2.2 2.1 2.6 
Alcohol (%)     
 Abstainer 17.8 18.6 19.9 21.1 
 ≤1 drink/day 70.7 69.8 69.5 67.0 
 >1 drink/day 11.5 11.6 10.6 11.9 
Smoking (%)     
 Current 7.9 7.8 7.5 8.1 
 Former 41.8 38.5 35.0 35.1 
 Never 50.3 53.7 57.5 56.8 
Education (%)     
 <HS 0.9 1.1 1.2 1.2 
 HS grad or some college 32.4 35.0 36.2 34.8 
 College grad 39.6 39.0 39.7 41.3 
 Postgraduate 27.1 24.9 22.9 22.7 
Hysterectomy (%)     
 No 65.6 65.5 65.0 66.8 
 Yes 34.4 34.5 35.0 33.2 
Non-whole/refined grains (oz/day; mean ± SD) 2.32 ± 1.26 2.39 ± 1.23 2.82 ± 1.34 3.94 ± 1.98 
Tomatoes (cups/day; mean ± SD) 0.24 ± 0.17 0.23 ± 0.17 0.25 ± 0.19 0.35 ± 0.28 
Other vegetables (cups/day; mean ± SD) 0.63 ± 0.51 0.44 ± 0.33 0.40 ± 0.29 0.45 ± 0.31 
Cruciferous vegetables (cups/day; mean ± SD) 0.23 ± 0.27 0.20 ± 0.24 0.22 ± 0.25 0.29 ± 0.41 
Cheese (cups/day; mean ± SD) 0.26 ± 0.21 0.28 ± 0.21 0.36 ± 0.24 0.66 ± 0.41 
Yogurt (cups/day; mean ± SD) 0.23 ± 0.28 0.10 ± 0.14 0.08 ± 0.12 0.06 ± 0.11 
Fish/shellfish high in ω-3 fatty acids (oz/day; mean ± SD) 0.18 ± 0.23 0.14 ± 0.17 0.13 ± 0.17 0.15 ± 0.22 
Fish/shellfish low in ω-3 fatty acids (oz/day; mean ± SD) 0.58 ± 0.63 0.40 ± 0.36 0.38 ± 0.34 0.42 ± 0.41 
Franks and luncheon meats (oz/day; mean ± SD) 0.37 ± 0.32 0.41 ± 0.33 0.51 ± 0.37 0.78 ± 0.59 
Nuts and seeds (oz/day; mean ± SD) 2.11 ± 2.26 1.31 ± 1.33 1.14 ± 1.17 1.20 ± 1.20 
Coffee (cups/day; mean ± SD) 2.19 ± 1.68 1.58 ± 1.40 1.19 ± 1.28 1.02 ± 1.25 

Abbreviations: HS, high school; MET, metabolic equivalent of task; PHT, postmenopausal hormone therapy.

Cox proportional hazards models were used to estimate HRs and 95% CIs for the association between the ERDP and postmenopausal breast cancer. The ERDP was evaluated as a continuous score (ranging from −8.32 to 4.67) and using quartiles, with the first quartile as the referent group representing diets hypothesized to have the lowest estrogenic risk. Multivariable models included age, total energy intake, BMI at baseline, BMI at age 30, postmenopausal hormone therapy (PHT) use, race/ethnicity, alcohol consumption, number of family members with a history of breast cancer, age at menarche, age at menopause, parity, and hysterectomy. Sensitivity analyses included: restricting to non-Hispanic whites, excluding participants with ≤ 1 year of follow-up, and excluding participants with more than one full family member diagnosed with breast cancer.

Population characteristics across quartiles of ERDP are shown in Table 1. The ERDP was not associated with any breast cancer outcomes, although the HRs for ER-negative increased slightly with increasing ERDP (Table 2).

Table 2.

HRs (95% confidence interval) for the relationship between the ERDP score and postmenopausal breast cancer in the Sister Study, 2003–2015

ERDP quartilesEstimate for continuous ERDP scorea
1st2nd3rd4th
Total breast cancer 
 No. of cases 520 474 484 490  
 Age adjusted 1.00 (ref) 0.92 (0.81–1.04) 0.98 (0.86–1.11) 1.03 (0.91–1.17) 1.01 (0.95–1.08) 
     P = 0.71 
 Age and energy adjusted 1.00 (ref) 0.93 (0.82–1.06) 0.98 (0.87–1.11) 1.01 (0.89–1.14) 1.00 (0.94–1.06) 
     P = 0.94 
 Multivariable adjustedb 1.00 (ref) 0.92 (0.81–1.04) 0.96 (0.85–1.09) 0.99 (0.87–1.12) 0.98 (0.92–1.05) 
     P = 0.61 
Invasive 
 No. of cases 393 368 350 373  
 Age adjusted 1.00 (ref) 0.95 (0.82–1.09) 0.94 (0.81–1.08) 1.05 (0.91–1.21) 1.01 (0.94–1.09) 
     P = 0.71 
 Age and energy adjusted 1.00 (ref) 0.97 (0.84–1.11) 0.95 (0.82–1.10) 1.01 (0.87–1.16) 0.99 (0.92–1.07) 
     P = 0.84 
 Multivariable adjustedb 1.00 (ref) 0.95 (0.82–1.09) 0.92 (0.79–1.06) 0.97 (0.84–1.12) 0.97 (0.90–1.04) 
     P = 0.37 
Invasive ER+ 
 No. of cases 308 268 250 272  
 Age adjusted 1.00 (ref) 0.88 (0.75–1.04) 0.86 (0.73–1.02) 0.99 (0.84–1.16) 0.98 (0.90–1.07) 
     P = 0.63 
 Age and energy adjusted 1.00 (ref) 0.90 (0.76–1.06) 0.87 (0.74–1.03) 0.94 (0.80–1.11) 0.96 (0.88–1.04) 
     P = 0.30 
 Multivariable adjustedb 1.00 (ref) 0.88 (0.75–1.04) 0.85 (0.71–1.00) 0.91 (0.77–1.08) 0.93 (0.86–1.02) 
     P = 0.11 
Invasive ER−      
 No. of cases 47 46 52 56  
 Age adjusted 1.00 (ref) 0.99 (0.66–1.49) 1.14 (0.77–1.70) 1.25 (0.85–1.85) 1.16 (0.95–1.41) 
     P = 0.14 
 Age and energy adjusted 1.00 (ref) 1.00 (0.66–1.50) 1.15 (0.77–1.71) 1.23 (0.83–1.82) 1.15 (0.94–1.40) 
     P = 0.18 
 Multivariable adjustedb 1.00 (ref) 0.99 (0.66–1.50) 1.14 (0.76–1.69) 1.21 (0.81–1.81) 1.14 (0.93–1.40) 
     P = 0.20 
Person years accumulated 66,545 66,112 65,100 64,201  
ERDP quartilesEstimate for continuous ERDP scorea
1st2nd3rd4th
Total breast cancer 
 No. of cases 520 474 484 490  
 Age adjusted 1.00 (ref) 0.92 (0.81–1.04) 0.98 (0.86–1.11) 1.03 (0.91–1.17) 1.01 (0.95–1.08) 
     P = 0.71 
 Age and energy adjusted 1.00 (ref) 0.93 (0.82–1.06) 0.98 (0.87–1.11) 1.01 (0.89–1.14) 1.00 (0.94–1.06) 
     P = 0.94 
 Multivariable adjustedb 1.00 (ref) 0.92 (0.81–1.04) 0.96 (0.85–1.09) 0.99 (0.87–1.12) 0.98 (0.92–1.05) 
     P = 0.61 
Invasive 
 No. of cases 393 368 350 373  
 Age adjusted 1.00 (ref) 0.95 (0.82–1.09) 0.94 (0.81–1.08) 1.05 (0.91–1.21) 1.01 (0.94–1.09) 
     P = 0.71 
 Age and energy adjusted 1.00 (ref) 0.97 (0.84–1.11) 0.95 (0.82–1.10) 1.01 (0.87–1.16) 0.99 (0.92–1.07) 
     P = 0.84 
 Multivariable adjustedb 1.00 (ref) 0.95 (0.82–1.09) 0.92 (0.79–1.06) 0.97 (0.84–1.12) 0.97 (0.90–1.04) 
     P = 0.37 
Invasive ER+ 
 No. of cases 308 268 250 272  
 Age adjusted 1.00 (ref) 0.88 (0.75–1.04) 0.86 (0.73–1.02) 0.99 (0.84–1.16) 0.98 (0.90–1.07) 
     P = 0.63 
 Age and energy adjusted 1.00 (ref) 0.90 (0.76–1.06) 0.87 (0.74–1.03) 0.94 (0.80–1.11) 0.96 (0.88–1.04) 
     P = 0.30 
 Multivariable adjustedb 1.00 (ref) 0.88 (0.75–1.04) 0.85 (0.71–1.00) 0.91 (0.77–1.08) 0.93 (0.86–1.02) 
     P = 0.11 
Invasive ER−      
 No. of cases 47 46 52 56  
 Age adjusted 1.00 (ref) 0.99 (0.66–1.49) 1.14 (0.77–1.70) 1.25 (0.85–1.85) 1.16 (0.95–1.41) 
     P = 0.14 
 Age and energy adjusted 1.00 (ref) 1.00 (0.66–1.50) 1.15 (0.77–1.71) 1.23 (0.83–1.82) 1.15 (0.94–1.40) 
     P = 0.18 
 Multivariable adjustedb 1.00 (ref) 0.99 (0.66–1.50) 1.14 (0.76–1.69) 1.21 (0.81–1.81) 1.14 (0.93–1.40) 
     P = 0.20 
Person years accumulated 66,545 66,112 65,100 64,201  

aHR corresponds to 1-unit increase in ERDP score.

bIncludes adjustment for age, TEI, BMI, BMI at age 30, PHT, race/ethnicity, alcohol use, number of family members with a history of breast cancer, age at menarche, age at menopause, parity, and hysterectomy.

Despite having a larger sample size with power to detect smaller associations than in PLCO, our investigation did not support previous studies observing an association between estrogen-based dietary patterns and postmenopausal breast cancer risk (3, 4). In PLCO, participants in the highest ERDP quartile were at 20% increased risk of invasive postmenopausal breast cancer (4). However, when stratified by family history of breast cancer, the association was limited to women without a family history. Null results presented here are in agreement with the stratified results in PLCO, and may be partially explained by the strong presence of family history, although excluding those with the strongest family history did not change results. Evidence for modification by family history in dietary studies of cancer is limited (8).

In addition to the potential for a true null or masking of an association by the ubiquitous familial risk, it is possible that differences in the FFQs used explain the null association. The FFQs used here and in the PLCO cohort to derive the ERDP differ in the number and description of the line items containing relevant foods. It is possible that these differences explain the different distributions of the scores between the two populations. The range of −8.23 to 4.67 in the Sister Study compared with a range of −4.52 to 6.58 in PLCO participants could indicate that participants in the Sister Study were not consuming diets with as much estrogenic potential, or that the FFQ in the Sister Study did not capture as many of the estrogen relevant foods. The lack of agreement between studies investigating dietary estrogenic potential support the need for research that evaluates differences across strata of family history, along with consideration of the impact of differing dietary assessment tools when comparing dietary patterns across study populations.

No potential conflicts of interest were disclosed.

Conception and design: M.A. Guinter, S.E. Steck

Development of methodology: M.A. Guinter, A.T. Merchant, S.E. Steck

Acquisition of data (provided animals, acquired and managed patients, provided facilities, etc.): D.P. Sandler

Analysis and interpretation of data (e.g., statistical analysis, biostatistics, computational analysis): D.P. Sandler, A.C. McLain, A.T. Merchant, S.E. Steck

Writing, review, and/or revision of the manuscript: M.A. Guinter, D.P. Sandler, A.T. Merchant, S.E. Steck

M.A. Guinter was supported in part by a grant from NIH, National Institute of General Medical Sciences (T32-GM081740). D.P. Sandler was supported by the Intramural Program of the NIH, National Institute of Environmental Health Sciences (Z01 ES-044005). S. Steck was supported by a grant from Susan G. Komen (GTDR17500160).

The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

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