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Dietary Patterns and Survival After Breast Cancer Diagnosis

From the University of California, Robert Wood Johnson Health and Society Scholars Program, San Francisco, CA; Simmons College; Department of Nutrition, Harvard School of Public Health; Channing Laboratory, Department of Medicine, Brigham & Women's Hospital; and Harvard Medical School, Boston, MA

Address reprint requests to Candyce Kroenke, ScD, University of California, 3333 California St, Suite 465, San Francisco, CA 94118; e-mail: ckroenke{at}berkeley.edu

	ABSTRACT

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION Authors' Disclosures of... REFERENCES

 
PURPOSE: There is little prior study of major dietary patterns and breast cancer survival.

METHODS: Patients included 2,619 Nurses' Health Study participants who were diagnosed with invasive breast cancer between 1982 and 1998 and completed a dietary questionnaire more than 1 year after diagnosis. Participants were followed through 2002 (median = 9 years). During follow-up, 414 patients died of any cause, 242 patients died of breast cancer, and 172 patients died from causes other than breast cancer. Women with in situ or metastatic disease at diagnosis were excluded. We used Cox proportional hazards models to evaluate prospective associations of prudent and Western dietary patterns assessed both before and after diagnosis with time to event after diagnosis.

RESULTS: In multivariate-adjusted analyses assessed after diagnosis, the Western and prudent dietary patterns were unrelated to all-cause or breast cancer mortality. However, compared with women with the lowest intake of the prudent dietary pattern, the relative risks (and 95% CIs) of death from causes other than breast cancer were 0.85 (95% CI, 0.53 to 1.35), 0.74 (95% CI, 0.45 to 1.21), 0.70 (95% CI, 0.42 to 1.17), and 0.54 (95% CI, 0.31 to 0.95; P = .03, from lowest to highest quintile of intake). In contrast, the Western dietary pattern was positively associated with this outcome (P = .04). Results for the assessment of dietary patterns before diagnosis were similar, except the prudent dietary pattern was unrelated to mortality.

CONCLUSION: A higher intake of the prudent pattern and a lower intake of the Western pattern may protect against mortality from causes unrelated to breast cancer.

	INTRODUCTION

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A considerable amount of research has examined the possible influence of diet on breast cancer survival, the bulk focusing on specific nutrients,^1-4 especially fat intake^4-9 or individual foods.^10,11 Intake of fruit and vegetables or nutrients typically found in fruit and vegetables have been related to better survival,^3,6,11 whereas associations of fat intake and survival have been mixed.^4-9 A recent article by Goodwin et al¹ suggested that extremes in intake may be detrimental for survival. In all likelihood, several aspects of diet influence breast cancer survival. However, there is little previous study examining dietary patterns and survival after breast cancer in a free-living population.

A few prior studies have explored differences in breast cancer survival among women consuming vegetarian and nonvegetarian diets, and associations have been mixed.^12-16 Unfortunately, these studies have not focused specifically on populations of women with breast cancer and the numbers of women with breast cancer in these studies have been small, ranging from five to 79 patients. Furthermore, investigators have failed to adjust for potentially important confounding variables, particularly those related to the experience of breast cancer. Key et al,¹⁷ in a meta-analysis, found no overall association between vegetarian diet and breast cancer mortality, but they examined survival after numerous disease outcomes and adjusted for age and smoking only. Furthermore, nonvegetarian diets may range in quality and a greater lack of specificity may hinder efforts to understand how diet contributes to survival after breast cancer.

It may therefore be more useful to study patterns of intake more consistent with what is considered to be related to health outcomes after a diagnosis of breast cancer. Previous studies have found whole grain¹⁸ and fruit and vegetable intake¹¹ to be related to a lower risk of mortality after breast cancer. Grain fiber intake has been associated with lower levels of estradiol,¹⁹ and previous results suggest a potential protective effect of grain fiber in breast cancer mortality.^18,20 In contrast, high consumption of animal fat^6,7,10 may jeopardize survival.

We previously identified two major dietary patterns by means of factor analysis.²¹ The prudent dietary pattern was characterized by a diet high in fruits, vegetables, whole grains, legumes, poultry, and fish, and the Western pattern was characterized by high intake of refined grains, processed and red meats, desserts, high-fat dairy products, and french fries. Several aspects of the prudent dietary pattern have been related to lower breast cancer mortality. Though most components of a Western diet have not been studied for their relationship to breast cancer survival, the Western pattern is characterized by a high glycemic load,²² which may promote weight gain and thus jeopardize survival.²³

We therefore hypothesized that a prudent dietary pattern would be associated with a lower risk of breast cancer mortality and total mortality and that a Western pattern would be associated with higher risks of these outcomes. With nearly 2 million breast cancer survivors in the United States,²⁴ it is important to determine factors that may improve survival.

	METHODS

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Nurses' Health Study Participants
The Nurses' Health Study (NHS) is a prospective study of 121,700 United States female nurses, 30 to 55 years of age at baseline in 1976. At baseline and during biennial follow-up periods, participants provided detailed lifestyle and medical history information through a mailed questionnaire.

In this study, we included 2,619 women who were diagnosed with invasive breast cancer between 1982 and 1998 and who completed a dietary questionnaire both in 1984 and at least 1 year after breast cancer diagnosis. Participants were followed through 2002. Women with in situ disease or metastatic breast cancer at diagnosis were excluded from the study. Metastatic cancer was defined as having a physician-confirmed diagnosis of metastatic breast cancer. Women with four or more positive nodes but lacking a complete metastatic work-up were also excluded because of concerns for occult metastatic disease. A complete metastatic work-up consisted of a negative chest x-ray (or chest computed tomography), bone scan, and liver function tests (or liver scan) or documentation from a treating physician that the patient did not have metastatic disease. We additionally eliminated recurrences (defined as a second cancer on a routine NHS follow-up if she reported lung, liver, bone, or brain cancer) and breast cancer deaths that occurred within a year of diagnosis to eliminate likely metastatic cases that were not classified as such by our initial definition. We further excluded women with previous cancer. For analyses of diet before breast cancer diagnosis, we included women diagnosed between 1984 and 2000 and followed up to 2002, with 2,524 responding to a dietary food frequency questionnaire (FFQ) within 4 years before diagnosis. To maximize the number of women in each analysis and reduce possible bias, we did not reduce the women to a common subset. Of the women who completed a dietary questionnaire after breast cancer diagnosis, 414 women died of any cause, 242 women died of breast cancer, and 172 women died from causes other than breast cancer during follow-up.

Data Collection
Measurement of breast cancer. In the NHS, incident breast cancer was ascertained by biennial mailing of the questionnaire to participants. For any report of breast cancer, written permission was obtained from study participants to review their medical records. Physicians, blinded to exposure information from questionnaires, subsequently reviewed medical records and pathology reports. Overall, 99% of self-reported invasive breast cancers for which medical records are obtained have been confirmed.

Measurement of mortality. Ascertainment of deaths in the NHS cohort included reporting by the family or postal authorities. Additionally, names of persistent nonresponders were searched in the National Death Index,²⁵ which is a reliable method in women with breast cancer.²⁶ Date of death was ascertained from death certificates. The cause of death was assigned by physician reviewers. In the case of a woman who died from a breast cancer not previously reported, medical records were obtained to record details of her breast cancer diagnosis. More than 98% of deaths in the NHS cohort have been identified by this method.²⁷

Mortality in this study was defined as breast cancer mortality if cause of death was listed on the death certificate as breast cancer. All-cause mortality was defined as death from any cause. Mortality from causes other than breast cancer was determined by excluding mortality from breast cancer. The primary outcome of interest in our analyses was all-cause mortality to avoid issues of interpretation owing to possible misclassification of cause of death.

Measurement of diet. Information on dietary intake was collected by FFQ. The questionnaire was designed to assess average food intake during the previous year, and standard portion size was given for each food item. Cohort members were asked to choose from nine possible frequency responses, ranging from "never" to "more than six times a day" for each food. Total caloric intake was calculated by summing up intakes from all foods.

To generate the dietary patterns, we used information from the FFQ administered in 1984, which had 116 items. Foods from the FFQ were classified into 38 food groups based on nutrient profiles or culinary usage. Foods that did not fit into any of the groups or that may represent distinctive dietary behaviors were left as individual categories (eg, pizza, tea, beer). Previous validation studies among members of the NHS cohort showed reasonably high correlations between nutrients assessed by the FFQ and multiple weeks of food records completed during the previous year, ranging from 0.45 to 0.58 for major nutrients including carbohydrate, protein, total fat, and total fiber.²⁸

Statistical Analyses
Dietary patterns were generated by factor analysis (principal components) on the basis of 38 food groups by means of the orthogonal rotation procedure.²⁹ This results in uncorrelated or independent factors, which are easier to interpret. The factor scores are standardized to have a mean of 0 and standard deviation of 1. We determined the number of factors to retain by eigenvalue (greater than 1), Scree test, and factor interpretability. This resulted in the selection of two patterns, which we called prudent and Western, consistent with dietary patterns characterized in other studies.^30-32 The factor score for each pattern was found by summing intakes of food groups weighted by factor loading,³³ and each individual received a factor score for each identified pattern. Factor analysis was conducted with SAS PROC FACTOR (SAS Institute Inc, Cary, NC).

We regressed food groups and energy-adjusted nutrients against quintiles of dietary patterns, adjusted for continuous age (Table 1). Additionally, we regressed potential confounding variables against quintiles of the dietary patterns (Table 2).

We conducted three sets of analyses. First, we evaluated survival outcomes and dietary patterns before breast cancer diagnosis by examining (1) the closest diet before diagnosis and (2) the cumulative average of diet before diagnosis. Furthermore, we analyzed (3) the single diet measured closest to and after breast cancer diagnosis among those who completed the diet at least 12 months after diagnosis to allow for completion of treatment. We did not examine dietary patterns after diagnosis using cumulative updating because of concerns with interpretation if low intake is due to an overall decrease in intake because of a recurrence. Our analyses focused primarily on diet after diagnosis, because once a woman is diagnosed with breast cancer, she cannot change lifestyle factors occurring before diagnosis. In addition to examining associations of dietary patterns with survival outcomes, we also examined associations of several individual food groups included in the summary dietary patterns including vegetables, fruit, whole grains, processed meat, high fat dairy, and desserts. We also examined associations with fiber and saturated fat intake because these are nutrients which are being examined most critically in an ongoing intervention study.³⁶

Results adjusted for age were compared with those obtained adjusting for multiple factors shown to be predictive of survival after breast cancer diagnosis in the NHS cohort including age, body-mass index (BMI), oral contraceptive use, menopausal status, age at menopause, use of postmenopausal hormone therapy (before diagnosis of breast cancer), breast cancer stage using the standard American Joint Committee on Cancer staging criteria (stage 1, 2, or 3),³⁷ chemotherapy, and hormonal therapy. We adjusted for parity and age at birth using Rosner's and Colditz's birth index, which enables fine adjustment for parity and age at each birth with the inclusion of a single, continuous variable.³⁸ We evaluated models with and without adjustment for dietary variables, including energy intake and alcohol intake. Adjustment for energy intake influenced the parameter estimates, but adjustment for alcohol intake did not. Therefore, we dropped alcohol intake from the analyses. We also adjusted for time elapsed between dietary assessments and time of diagnosis.

We further evaluated models stratified by variables including breast cancer stage, hormone receptor status (estrogen-receptor [ER] –negative, defined as both ER- and progesterone-receptor [PR] –negative; ER-positive, defined as either ER- or PR-positive), treatment regimen (chemotherapy, tamoxifen), menopausal status (premenopausal v postmenopausal), and overweight status at baseline (defined as BMI 25 kg/m²). Interaction terms were computed for continuous dietary factors and dichotomous versions of each of these variables and were evaluated with Wald tests. We additionally examined the cross-classification (ie, joint effect) of categories of prudent dietary patterns with Western dietary patterns. In doing so, we combined quintiles 1 and 2 and quintiles 4 and 5 into single categories.

Finally, we conducted several sensitivity analyses. We performed analyses with and without eliminating all cases of prior cancer. We also examined associations including recurrences and breast cancer deaths that occurred within a year of diagnosis. We initially excluded women with metastatic cancer to avoid bias due to confounding by indication. However, this is more of a concern in the analysis of postdiagnosis diet. Therefore, to attempt to determine whether associations might vary with the inclusion of women with metastatic cancer, we conducted an additional analysis of prediagnosis diet and survival, including these women.

All tests of statistical significance were two-sided. This research was approved by the institutional review board at Brigham and Women's hospital in Boston, MA.

	RESULTS

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Women with high prudent dietary pattern scores consumed higher amounts of fruit, vegetables, whole grains, and low-fat dairy products. They also consumed higher amounts of protein and fiber and lower amounts of trans-unsaturated and saturated fats and had a diet with a lower glycemic load. In contrast, women with high Western dietary pattern scores consumed higher amounts of refined grains, processed meat, red meat, high-fat dairy, and desserts. They also consumed less protein and fiber, higher trans- and saturated fats, and had a higher glycemic load (Table 1).

Women with high prudent dietary pattern scores tended to engage in typically healthy behaviors. They were less likely to smoke, more likely to use vitamin supplements, and had higher physical activity. In contrast, women with high Western pattern scores were more likely to be current smokers and were less likely to use vitamin supplements (Table 2). Variables related to breast cancer diagnosis, including stage and treatment with chemotherapy, were generally unrelated to dietary patterns.

Prediagnosis Diet
In both age- and multivariate-adjusted analyses of single diet closest to and before breast cancer diagnosis, prudent diet was unrelated to survival (data not shown). In contrast, those with a higher intake of the Western diet had a slightly higher (nonsignificant) risk of all-cause mortality and a significantly higher risk of mortality from causes other than breast cancer (Table 3). Associations were similar with cumulative updated diet before breast cancer diagnosis (data not shown).

Sensitivity Analyses
Results did not vary with the inclusion of women with prior cancer or with inclusion of women who recurred or died within the first year after diagnosis. Furthermore, results were unchanged in analyses of prediagnosis diet and outcomes when we included women with metastatic breast cancer.

	DISCUSSION

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION Authors' Disclosures of... REFERENCES

 
After breast cancer diagnosis, adherence to a prudent dietary pattern was unrelated to all-cause mortality but was inversely related to mortality from causes other than breast cancer. The Western pattern was similarly but positively associated with mortality from causes other than breast cancer. Prudent dietary pattern before breast cancer diagnosis was not associated with survival, though the Western dietary pattern was positively associated with mortality from causes other than breast cancer after a diagnosis of breast cancer. Major dietary patterns were unrelated to breast cancer mortality. Although unrelated to breast cancer–specific survival, a higher intake of the prudent pattern and a lower intake of the Western pattern may protect against mortality from causes unrelated to breast cancer.

Little research has examined major dietary patterns and survival after breast cancer. We previously found a lack of association between dietary patterns and incidence of postmenopausal breast cancer,³⁹ and Key et al¹⁷ found no association between vegetarian diet and breast cancer survival. Because several aspects of the prudent diet have been associated with improved breast cancer survival,²⁰ we were somewhat surprised that the prudent dietary pattern was not more strongly related to breast cancer survival. We considered that it may be more difficult to detect an effect in the noise of other characteristics of this diet. However, in analyses of specific food groups, including whole grains, fruit and vegetables, or fiber or saturated fat, we found little evidence that consumption of these foods or nutrients was related to breast cancer survival. This did not seem to be due to overadjustment; SEs changed little with multivariate-adjustment. Although these foods and nutrients have been associated with survival in the past in some studies, this has not been true in all studies, and even significant associations have been modest.²⁰

We also considered that the lack of association of the prudent dietary pattern with breast cancer-specific survival may be due to the possibility that associations should be characterized as other than linear. In a previous study, Goodwin et al¹ found an apparent U-shaped association between several nutrients, including protein, oleic acid, cholesterol, polyunsaturated-saturated fat ratio, percentage of calories from fat, and percentage of calories from carbohydrates with breast cancer survival. However, we found no evidence that the risk of breast cancer mortality was lower in women with intermediate intakes of the prudent dietary pattern.

Rather, major diet patterns seemed to distinguish those more likely to die after breast cancer from causes unrelated to breast cancer. A higher intake of the prudent pattern has been associated with a lower risk of coronary heart disease,²¹ stroke,⁴⁰ plasma biomarkers of obesity,⁴¹ and inflammation and endothelial dysfunction.⁴² In contrast, a higher intake of the Western pattern has been associated with a higher risk of coronary heart disease,²¹ diabetes,⁴³ stroke,⁴⁰ and intermediate biomarkers of these outcomes.^41,42 High insulin levels, obesity,⁴⁴ and inflammation⁴⁵ have each been associated with an elevated risk of colorectal⁴⁶ and other cancers. Among those who did not die of breast cancer and for whom we had cause of death, 22% died related to cardiovascular causes (International Classification of Diseases-9 390-448), 45% died of other cancer (International Classification of Diseases-9 140-208), and the other 33% died of varied causes not related to cancer or cardiovascular disease. Our results are consistent with an influence of dietary patterns on cardiovascular outcomes and with cancer outcomes with similar underlying causes.

Strengths of this study include longitudinal analysis, the ability to stratify by breast cancer-specific factors, and careful control for possible confounding variables. Most studies have examined diet either before or after breast cancer survival. Ours is among the few to be able to examine how diet before and after diagnosis may influence survival.

Limitations include lack of complete information on treatment and severity. This was due in part to the inclusion of women in the analysis for whom we were unable to obtain medical records. This was additionally a problem for women diagnosed with breast cancer in the early 1980s when information on nodal involvement was not regularly collected. Because of this reason, we were unable to construct the variable breast cancer stage for women diagnosed with breast cancer during this time. Nevertheless, there was little difference in the distribution of most breast cancer–related variables by quintiles of dietary patterns, and a subanalysis excluding women without complete information on these factors did not substantially alter results.

Although previous studies show our ability to rank individuals on aspects of diet,⁴⁷ we are unable to estimate intake accurately, which limits our ability to evaluate the potential impact of change in diet before and after breast cancer diagnosis with subsequent outcomes. Observational studies with more complete assessment of dietary intake before and after diagnosis may ultimately be better able to address this question. Additionally, trials currently underway will be able to provide direct insights into the impact of absolute intake of fruit, vegetables, fiber, and fat after diagnosis on survival.^5,36 Initial results of the Women’s Intervention Nutrition Study (WINS) trial indicate a possible survival advantage for a dietary fat reduction after a breast cancer diagnosis.⁴⁸

Another limitation is that despite physician review of records, we cannot rule out the possibility that for some, cause of death may have been misclassified. Indeed, misclassification of cause of death is an ongoing issue in most studies of cause-specific mortality. Given our significant findings with causes of death other than breast cancer, certainty about cause of death is desirable. Nevertheless, the consistency of these findings with prior findings of dietary patterns and breast cancer³⁹ as well as with cardiovascular and other cancer outcomes^21,40,49 provides some reassurance about the integrity of our findings.

In summary, consistent with previous studies of dietary patterns and cardiovascular outcomes, dietary patterns were associated with mortality from causes other than breast cancer, suggesting that women may wish to adopt a more prudent lifestyle pattern and reduce intake of a Western pattern to improve longevity and overall health.

	Authors' Disclosures of Potential Conflicts of Interest

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION Authors' Disclosures of... REFERENCES

 
The authors indicated no potential conflicts of interest.

	NOTES

 
Supported by grant Nos. CA87969 and CA095589 from the National Cancer Institute, National Institutes of Health, Bethesda, MD.

Authors' disclosures of potential conflicts of interest are found at the end of this article.

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Submitted March 22, 2005; accepted September 30, 2005.

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