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Changes in diet quality in a randomized weight loss trial in breast cancer survivors: the lifestyle, exercise, and nutrition (LEAN) study

Changes in diet quality in a randomized weight loss trial in breast cancer survivors: the... www.nature.com/npjbcancer ARTICLE OPEN Changes in diet quality in a randomized weight loss trial in breast cancer survivors: the lifestyle, exercise, and nutrition (LEAN) study 1 1 2 1,3 3,4 1,3 1,3 Chelsea Anderson , Maura Harrigan , Stephanie M George , Leah M Ferrucci , Tara Sanft , Melinda L Irwin and Brenda Cartmel Obesity is associated with increased breast cancer recurrence and mortality. Though some post-diagnosis weight loss interventions have achieved weight loss outcomes, it is unclear whether they also improve diet quality. In the Lifestyle, Exercise, and Nutrition (LEAN) study, overweight or obese breast cancer survivors were randomized to either usual care group (n = 33) or the 6-month lifestyle intervention (n = 67). Dietary intake was assessed at baseline and 6 months using a validated food frequency questionnaire, and overall diet quality was calculated using the Healthy Eating Index (HEI)-2010 (range 0–100). Intervention effects on diet were evaluated with generalized linear models. Among the 81 participants (51 intervention, 30 usual care) with dietary data, the mean baseline HEI score was 70.5 (s.d. = 8.8) and was improved at 6 months (intervention group = 6.8 point increase vs usual care = 3.1, P = 0.09). Intervention group participants achieved greater reductions in percent of energy from total fat (−4.2% vs − 1.2%; P = 0.013) and saturated fat (−2.2% vs − 1.1%; P = 0.003), and greater increases in fiber (4.8 g per 1000 kcal vs 1.3 g per 1000 kcal; P = 0.007) and fruit (0.5 servings vs 0.0 servings; P = 0.006) intake. Intervention group participants who lost ⩾ 5% body weight (n = 27) demonstrated significantly greater improvements in HEI score (10.4 vs 2.8) than those who lost o5% (n = 23). The intervention increased fruit and fiber intake and decreased percent energy from fat, and those with greater weight loss achieved greater increases in overall diet quality. These findings support the ability of a weight loss intervention to improve diet among breast cancer survivors. npj Breast Cancer (2016) 2, 16026; doi:10.1038/npjbcancer.2016.26; published online 24 August 2016 INTRODUCTION 2010 Dietary Guidelines for Americans and has been found to be a valid and reliable measure of diet quality. Though research to With advances in early detection and treatment, the 5-year date is limited, existing studies suggest that higher diet quality is survival rate for breast cancer has increased to almost 90% for all stages combined. Yet despite these gains, breast cancer remains not associated with breast cancer mortality, but is associated with a the second leading cause of cancer deaths among US women. reduction in deaths from non-breast cancer causes among breast 12–14 Among breast cancer survivors, obesity at diagnosis is associated cancer survivors. While some previous studies have assessed with an increased risk of disease recurrence and both all-cause post-intervention changes in dietary components among breast 15–22 and breast cancer-specific mortality. Weight gain post diagnosis cancer survivors, few have evaluated changes in overall diet 4–6 23,24 may also be associated with a poor prognosis. The majority of quality. This is an important area to explore, as changes in diet breast cancer patients gain weight while undergoing treatment, quality may be independently associated with improvements in and many continue to gain weight in the years following the long-term health of breast cancer survivors. diagnosis. Breast cancer survivors are also at an increased risk The Lifestyle, Exercise, and Nutrition (LEAN) study was a of cardiovascular disease and diabetes relative to the general randomized controlled trial of a 6-month weight loss intervention population, both conditions related to being overweight or 25 among overweight and obese breast cancer survivors. Modeled obese. Weight loss and/or weight maintenance is thus an 26 after the successful Diabetes Prevention Program (DPP), the important goal for women following breast cancer diagnosis. LEAN intervention consisted of a series of either in-person or A recent systematic review documented the feasibility and telephone-based counseling sessions that encouraged weight loss effectiveness of comprehensive weight loss interventions for 9 through both physical activity and achieving or maintaining a breast cancer survivors. Although successful interventions have healthy diet. For the primary outcome, participants randomized to included a dietary component, it is unclear whether weight loss is the LEAN intervention achieved significantly greater weight loss accompanied by improvements in diet quality or simply a decrease than those assigned to a control group (6.4% vs 2.0%), as has been in caloric intake and increase in energy expenditure. A focus on reported previously. In this report, we present change in diet diet quality, as opposed to individual foods and nutrients, accounts quality and specific dietary components over the 6-month LEAN for the potentially synergistic effects of foods and food patterns on study in the intervention group compared with the control group. health. The Healthy Eating Index 2010 (HEI-2010) aligns with the 1 2 Department of Chronic Disease Epidemiology, Yale School of Public Health, New Haven, CT, USA; Office of Disease Prevention, National Institutes of Health, Bethesda, MD, USA; 3 4 Department of Internal Medicine, Yale Cancer Center, New Haven, CT, USA and Yale School of Medicine, New Haven, CT, USA. Correspondence: B Cartmel (brenda.cartmel@yale.edu) Received 11 February 2016; revised 10 June 2016; accepted 21 July 2016 Published in partnership with the Breast Cancer Research Foundation Diet quality changes in breast cancer survivors C Anderson et al RESULTS Table 1. Baseline participant characteristics Baseline characteristics by intervention group are presented in Table 1. In both the usual care and intervention groups, the Usual care Intervention P value majority of participants were white, married, postmenopausal, and (n = 30) n (%) (n = 51) n (%) well-educated. Baseline characteristics were similar between the Age (mean± s.d.) 57.90± 7.41 59.24± 7.15 0.426 intervention and the usual care groups with the exception of BMI (mean± s.d.) 33.99± 7.84 32.78± 6.40 0.453 alcohol intake, which was significantly higher in the intervention White 27 (90.0) 47 (94.0) 0.667 group (Po0.008). Over the 6-month intervention, average Latino 0 (0.0) 2 (3.9) 0.528 percentage of body weight lost was 6.4% in the intervention College graduate 20 (66.7) 35 (68.6) 0.855 group and 2.0% in the usual care group (Po0.01). Currently married 17 (56.7) 34 (66.7) 0.368 Table 2 shows the average HEI score and individual dietary Postmenopausal 23 (76.7) 42 (82.4) 0.535 Ever smoker 13 (43.3) 20 (39.2) 0.716 components by group at baseline and 6 months. At baseline, the Drink alcohol 23 (76.7) 48 (96.0) 0.008 average HEI score was 70.17 (s.d. = 8.51) in the intervention group 1st degree family 9 (30.0) 16 (32.0) 0.852 and 71.08 (s.d. = 9.27) in the usual care group (P=0.788). At history of breast cancer 6 months, the HEI score improved by 6.80 (s.d. = 10.06) in the Stage 0.946 intervention group. This was nearly double the 3.05 (s.d. = 8.03) 0 6 (20.0) 8 (15.7) increase in the usual care group, though the difference in change in I 15 (50.0) 26 (51.0) HEI score between groups was not statistically significant (P=0.09). II 6 (20.0) 13 (25.5) Significant differences between groups were observed for III 2 (6.7) 3 (5.9) Unknown 1 (3.3) 1 (2.0) change over the 6-month study for four of the eight diet Treatment 0.868 components targeted by our intervention (Table 2). Relative to the Neither chemo nor 5 (16.7) 7 (13.7) usual care group, the intervention group reported greater radiation reductions in percent energy from total fat and from saturated Radiation only 12 (40.0) 17 (33.3) fat. Specifically, percent energy from total fat decreased by 4.19% Chemo only 4 (13.3) 9 (17.7) (s.d. = 6.49) in the intervention group, as compared with a 1.12% Both radiation and 9 (30.0) 18 (35.3) (s.d. = 6.72) reduction in the usual care group (P = 0.01). Percent chemo energy from saturated fat decreased by 2.20% (s.d. = 2.39) in the Current endocrine 24 (82.8) 40 (83.3) 0.948 therapy intervention group and by 1.05% (s.d. = 2.16) in the usual care group (P = 0.003). The intervention group also reported greater a 2 T-tests for continuous variables and χ -test for categorical variables. increases in fiber intake and fruit servings at 6 months. Fiber grams increased by 4.84 g per 1,000 kcal (s.d. = 4.72) among the intervention group and 1.28 g per 1,000 kcal (s.d. = 4.21) among frequently assessed in weight loss intervention studies. The HEI the usual care group (P = 0.007). Fruit servings increased by 0.66 emphasizes consumption of more fruits, vegetables, and whole servings (s.d. = 1.66) in the intervention group and decreased by grains and less refined grains, sodium, and empty calories. High 0.37 servings (s.d. = 1.51) in the usual care group (P = 0.006). For scores on the HEI reflect diets with an appropriate balance of food the remaining dietary intake variables—including calories, fat groups, rather than individual nutrients, thus allowing for the grams, added sugar, and vegetables servings—the intervention potentially synergistic effects of individual dietary components to group improved to a greater extent than the usual care group, but be evaluated. The average HEI score among LEAN participants at differences between groups were not statistically significant. Within group associations between percent weight loss and baseline was ~ 70, comparable to that found among participants change in HEI score are shown in Table 3. There was a significant who voluntarily enroll in large diet studies, such as the NIH-AARP Diet and Health Study. On the other hand, a recent study using correlation between percent weight loss and change in HEI in data from the National Health and Nutrition Examination Survey the intervention group (r = − 0.42 P = 0.002) with the increase in (NHANES) reported an average HEI-2010 score of only 51 among HEI score greater among participants who lost at least 5% of breast cancer survivors, suggesting that LEAN participants were their initial body weight, relative to those who lost o5% (10.35 vs already eating relatively healthy diets. 2.82, P = 0.01). In the general population, higher scores on the HEI-2010 have been associated with reduced all-cause mortality, as well as DISCUSSION cardiovascular disease and cancer-specific mortality among 31,33,34 This study evaluated the effect of a 6-month lifestyle and weight women. Using the previous version of the HEI, the HEI-2005, loss intervention on diet quality and selected dietary components an inverse association between post-diagnosis diet quality and all- among overweight and obese breast cancer survivors. Results cause mortality has also been documented among breast cancer demonstrate that the LEAN intervention, which resulted in an survivors. However, the relationship between diet quality and average 6.4% weight loss, was successful in increasing fruit and breast cancer-specific survival remains unclear, as few studies have 12–14 fiber consumption and in decreasing percent energy from both fat examined such associations. To our knowledge, the impact of and saturated fat. Though differences between intervention and post-diagnosis changes in diet quality on breast cancer outcomes usual care groups were not significant, changes in diet quality as has also not been explored. At 6 months, participants in the LEAN intervention improved their HEI-2010 score by an average of 6.8 assessed by the HEI-2010 were in the expected direction. Of note, intervention participants who lost more weight had greater points, and those who lost at least 5% of their initial body weight increases in HEI score, suggesting that improvements in overall demonstrated an increase of over 10 points. Further studies are diet quality were an additional benefit of the intervention among needed to evaluate the impact of such changes—both alone and in women who achieved successful weight loss. conjunction with weight loss—on outcomes among breast cancer Previous reports have documented post-intervention changes survivors. in other diet quality indices among survivors of breast cancer and Notably, we also observed significant changes in components 23,24,27–29 other cancer types. However, this report is unique for the of the diet that were specifically emphasized in the structure of focus on change in the HEI-2010, the most recent version of the the LEAN intervention. Decreasing energy intake from fat was HEI, in addition to the change in specific dietary components emphasized as a way to reduce caloric intake and promote weight npj Breast Cancer (2016) 16026 Published in partnership with the Breast Cancer Research Foundation Diet quality changes in breast cancer survivors C Anderson et al Table 2. Comparison of dietary components and HEI-2010 scores between intervention (n= 51) and usual care (n= 30) Baseline (mean ± s.d.) 6 months (mean ± s.d.) Change (mean ± s.d.) P value Calories 0.561 Intervention 1,836.03± 784.92 1,481.07± 466.74 − 354.96± 725.65 Usual care 1,762.25± 747.39 1,522.64± 674.85 − 239.61± 680.25 % Energy from fat 0.013 Intervention 32.22± 8.26 28.03± 6.26 − 4.19± 6.49 Usual care 31.99± 6.92 30.87± 5.76 − 1.12± 6.72 Fat (g) 0.096 Intervention 67.84± 37.40 46.43± 19.84 − 21.41± 34.37 Usual care 64.10± 32.21 52.99± 25.09 − 11.12± 27.93 % energy from saturated fat 0.003 Intervention 10.29± 2.91 8.09± 2.24 − 2.20± 2.39 Usual care 10.34± 2.73 9.29± 1.79 − 1.05± 2.16 Added sugar (gm per 1,000 kcal) 0.084 Intervention 30.04± 15.38 25.14± 10.18 − 4.90± 14.95 Usual care 32.76± 10.72 30.33± 13.47 − 2.44± 9.37 Fiber (gm per 1,000 kcal) 0.007 Intervention 12.22± 3.84 17.06± 4.98 4.84± 4.72 Usual care 12.56± 4.29 13.83± 4.27 1.28± 4.21 Fruit servings 0.006 Intervention 2.18± 1.43 2.84± 1.81 0.66± 1.66 Usual care 2.35± 1.77 1.98± 1.33 − 0.37± 1.51 Vegetable servings 0.106 Intervention 2.79± 1.54 3.32± 1.74 0.53± 1.58 Usual care 2.72± 1.79 2.74± 2.02 0.02± 1.20 HEI-2010 score 0.092 Intervention 70.17± 8.51 76.97± 9.80 6.80± 10.06 Usual care 71.08± 9.27 74.13± 9.09 3.05± 8.03 Abbreviation: HEI, healthy eating index. P value for difference between groups in change in intake (6 months—baseline), controlling for baseline. survivors. Furthermore, the LEAN study was not powered to detect Table 3. Change in HEI score by percentage of weight loss changes in diet quality, as this was not a primary outcome. Larger studies are needed to evaluate the impact of weight loss Weight loss o5% Weight loss ⩾ 5% P value interventions, such as the LEAN intervention, on HEI scores and Intervention 2.82± 7.20 10.35± 11.09 0.010 ultimately the impact of diet quality on recurrence and survival. Usual care 2.38± 8.15 4.89± 7.90 0.268 Even though LEAN participants may have been eating a healthier diet compared with the general population, as evidenced by their Abbreviation: HEI, healthy eating index. relatively high HEI scores at enrollment, we still saw modest P value for difference in change in HEI score by weight loss %, within each group, controlling for baseline HEI score. improvements in the intervention group for HEI score and significant Intervention group: weight loss o5% (n= 23); weight loss ⩾ 5% (n= 27). improvements for diet components targeted by our intervention. Usual care group: weight loss o5% (n= 22); weight loss ⩾5% (n = 8). These dietary changes could be attributed to the fact that women who volunteer for intervention trials are also often more educated and more motivated than a more general population sample. However, a breast cancer diagnosis may represent a teachable loss, while the increases in fruit and fiber consumption were moment, and thus many survivors may be highly motivated to make consistent with the recommendation to eat a predominately lifestyle changes, such as improving their diet. plant-based diet. Though not significantly different from the usual In summary, the efficacious LEAN weight loss intervention care group, other aspects of diet, including intakes of vegetables improved several aspects of diet among breast cancer survivors. and added sugars, also improved in the intervention group compared with the usual care group. While some studies have The changes observed reflect key recommendations of the dietary suggested that diets low in saturated fat and high in fruits and counseling in the intervention. Diet quality also changed favorably vegetables are associated with improved breast cancer prognosis among intervention participants, particularly those who lost a and survival, such associations have not been demonstrated greater percentage of their body weight. These findings suggest 35,36 consistently. However, such diets have been shown to that weight loss interventions can favorably impact participants’ 31,33,34 decrease mortality from heart disease, the most common diet quality, with potential implications for the overall health and cause of death in breast cancer survivors. longevity of breast cancer survivors. Future trials should be Though this study has several strengths, including the designed to assess the impact of dietary change on long-term randomized design and counseling from a registered dietician outcomes such as recurrence and survival. to target dietary changes, there are also potential limitations. One limitation is measurement error inherent to the food frequency MATERIALS AND METHODS questionnaire (FFQ). In addition, the use of an FFQ to assess dietary change may lead to differential reporting between Participants intervention and control groups. LEAN participants were also Women who had a body mass index (BMI)⩾ 25.0 kg/m and had been fairly homogenous with respect to sociodemographic character- diagnosed with Stage 0 to III breast cancer in the 5 years prior to istics such as age and race/ethnicity, and thus our results may not enrollment were eligible for the study. Eligible participants also had be generalizable to other more diverse groups of breast cancer completed chemotherapy and/or radiation and were physically able to Published in partnership with the Breast Cancer Research Foundation npj Breast Cancer (2016) 16026 Diet quality changes in breast cancer survivors C Anderson et al exercise. Women had to be accessible by telephone and be able to read components or 1 ounce (1 ounce = 28.35 g) in the grains or protein foods and communicate in English. Details of recruitment procedures can be components. found elsewhere. Briefly, the study was advertised in the Breast Center at The HEI-2010 is calculated by summing 12 component scores, each of Smilow Cancer Hospital at Yale-New Haven and the Yale Cancer Center which reflects recommendations in the 2010 Dietary Guidelines for Survivorship Clinic. Women self-referred and were recruited between 1 Americans. Component scores are calculated using a density-based June 2011 and 30 December 2012. The study was approved by the Yale approach (i.e., per 1,000 kcal or percent of total energy), and higher scores School of Medicine Human Investigation Committee. for all components reflect closer adherence to the Dietary Guidelines. One One hundred eligible women agreed to randomization and gave component, empty calories (calories from solid fats and added sugars that informed consent. Using a random permuted block design, participants add no nutrients) is scored from 0 to 20. Five components (whole grains, were randomly assigned to one of the following groups: in-person dairy, fatty acids, refined grains, and sodium) are scored from 0 to 10, and counseling, telephone-based counseling, or usual care. Eighty-one women six components (total fruit, whole fruit, total vegetables, greens and beans, (81%), (51 intervention, 30 usual care) had complete dietary data and were total protein foods, and seafood and plant proteins) are scored from 0 to 5. included in the analysis. Components to be consumed in moderation—refined grains, sodium, and empty calories—are reverse scored. Thus the possible range for the total HEI score (the sum of the 12 components) is 0–100. For each participant Intervention groups in the LEAN study, the 12 HEI component scores and a total HEI score were For both the in-person and telephone-based counseling groups, the calculated for both the baseline and 6-month dietary assessments. In intervention consisted of 11 individualized sessions with a registered addition to HEI scores, diet components that were specifically emphasized dietician. The content of the weight loss program was similar for both in the LEAN intervention were also used to evaluate participants’ diet groups, with only the delivery being different (in-person vs telephone quality. These diet components were derived from the FFQ and included counseling). The sessions, ~ 30 min in duration, occurred each week for the calories, percent energy from fat, percent energy from saturated fat, added first month, followed by bimonthly sessions in months 2 and 3 and sugar, fiber, fruit servings, and vegetable servings. monthly sessions in months 4–6. The intervention components were adapted from the DPP, as well as Statistical analysis weight management materials from the American Institute for Cancer Research (AICR), the American Cancer Society, and the National Cancer Due to the similarity of intervention components and weight loss Institute. Dietary recommendations were also drawn from the Dietary outcomes between the in-person and telephone-based counseling Guidelines 2010. The primary goal of the intervention was for participants groups, these two groups were combined for the purposes of these to achieve a weight loss of 10% of initial body weight. A combination of analyses. Characteristics of the usual care group and intervention groups reduced caloric intake, increased physical activity, and behavior therapy was were compared using t-tests for continuous variables and Χ -tests or emphasized, with strategies based on constructs of the Social Cognitive Fisher's exacts tests for categorical variables. Theory. For the diet portion of the intervention, participants set goals for For the HEI score and all dietary intake variables, the main outcome was energy intake in the range of 1,200–2,000 kcal per day (based on baseline changed over the intervention period, which was calculated as the 6- weight) and were advised to limit fat consumption to 25% of total energy month value minus the baseline value. To test for differences in average intake. Other targets included increasing fiber intake to 25 g per day and change between the two groups, generalized linear models were used reducing consumption of added sugars. Eating a largely plant-based diet with adjustment for baseline values. To assess whether a change in HEI was also emphasized, with the recommendations to eat a minimum of five score was associated with weight loss, participants within each group were servings of fruits and vegetables per day, and to reduce portion sizes of categorized by their percentage of weight lost (o5% or ⩾ 5%) over the meat and other animal products. course of the intervention period. Analysis of variance was used to To track their personal intake of various dietary components, such as fat compare the change in HEI score by weight loss percent within each and fiber, women in the intervention groups recorded their daily food group, with adjustment for baseline HEI score. consumption in a log book developed for the study. The women were also asked to weigh themselves weekly at home using a scale provided for them. ACKNOWLEDGMENTS We are indebted to the participants for their dedication and time to the LEAN study. Usual care group This study was supported by the AICR and in part by a grant from the Breast Cancer Research Foundation. Also supported in part by the Yale Cancer Center Support Participants assigned to the usual care group received AICR nutrition and Grant (CCSG) P30 CA016359 and the CTSA Grant Number UL1 TR000142 from the physical activity brochures. They were also referred to the Yale Cancer National Center for Advancing Translational Science (NCATS), a component of the Center Survivorship Clinic, which offers a two-session weight management National Institutes of Health (NIH). The authors assume full responsibility for analyses program. Following study completion at 6 months, participants in the and interpretation of these data. usual care group were offered all educational material provided to participants in the counseling groups, as well as an in-person counseling session. CONTRIBUTIONS M.L.I., B.C., M.H., and L.M.F. conceived and designed the study. M.H. recruited the Assessments subjects, conducted data collection, and delivered the intervention. C.A. conducted Medical history and demographic data were collected via questionnaire at the data analysis. S.M.G. and L.M.F. assisted in the data analysis. C.A., B.C., M.L.I., S.M. baseline. Anthropometric measures, including weight and height, were G., M.H., L.M.F., T.S., and C.A. participated in interpreting the data and writing the assessed by study staff during clinic visits at both baseline and 6 months. manuscript. Dietary intake was assessed at baseline and 6 months using a 120-item FFQ. This instrument was developed for the Women’s Health Initiative (WHI) and has been validated against 4-day food records and 24-h dietary COMPETING INTERESTS recalls. The nutrient database used to analyze the WHI FFQ was derived The authors declare no conflict of interest. from the Nutrition Data Systems for Research, version 2005 (the University 41,42 of Minnesota, Minneapolis, MN, USA). 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Daughters and Mothers Against Breast Cancer article are included in the article’s Creative Commons license, unless indicated (DAMES): main outcomes of a randomized controlled trial of weight loss in otherwise in the credit line; if the material is not included under the Creative Commons overweight mothers with breast cancer and their overweight daughters. Cancer license, users will need to obtain permission from the license holder to reproduce the 120, 2522–2534 (2014). material. To view a copy of this license, visit http://creativecommons.org/licenses/ 25. Harrigan, M. et al. Randomized trial comparing telephone versus in-person weight by/4.0/ loss counseling on body composition and circulating biomarkers in women treated for breast cancer: the lifestyle, exercise, and nutrition (LEAN) study. J. Clin. Oncol. © The Author(s) 2016 34,669–676 (2016). Published in partnership with the Breast Cancer Research Foundation npj Breast Cancer (2016) 16026 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png npj Breast Cancer Springer Journals

Changes in diet quality in a randomized weight loss trial in breast cancer survivors: the lifestyle, exercise, and nutrition (LEAN) study

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www.nature.com/npjbcancer ARTICLE OPEN Changes in diet quality in a randomized weight loss trial in breast cancer survivors: the lifestyle, exercise, and nutrition (LEAN) study 1 1 2 1,3 3,4 1,3 1,3 Chelsea Anderson , Maura Harrigan , Stephanie M George , Leah M Ferrucci , Tara Sanft , Melinda L Irwin and Brenda Cartmel Obesity is associated with increased breast cancer recurrence and mortality. Though some post-diagnosis weight loss interventions have achieved weight loss outcomes, it is unclear whether they also improve diet quality. In the Lifestyle, Exercise, and Nutrition (LEAN) study, overweight or obese breast cancer survivors were randomized to either usual care group (n = 33) or the 6-month lifestyle intervention (n = 67). Dietary intake was assessed at baseline and 6 months using a validated food frequency questionnaire, and overall diet quality was calculated using the Healthy Eating Index (HEI)-2010 (range 0–100). Intervention effects on diet were evaluated with generalized linear models. Among the 81 participants (51 intervention, 30 usual care) with dietary data, the mean baseline HEI score was 70.5 (s.d. = 8.8) and was improved at 6 months (intervention group = 6.8 point increase vs usual care = 3.1, P = 0.09). Intervention group participants achieved greater reductions in percent of energy from total fat (−4.2% vs − 1.2%; P = 0.013) and saturated fat (−2.2% vs − 1.1%; P = 0.003), and greater increases in fiber (4.8 g per 1000 kcal vs 1.3 g per 1000 kcal; P = 0.007) and fruit (0.5 servings vs 0.0 servings; P = 0.006) intake. Intervention group participants who lost ⩾ 5% body weight (n = 27) demonstrated significantly greater improvements in HEI score (10.4 vs 2.8) than those who lost o5% (n = 23). The intervention increased fruit and fiber intake and decreased percent energy from fat, and those with greater weight loss achieved greater increases in overall diet quality. These findings support the ability of a weight loss intervention to improve diet among breast cancer survivors. npj Breast Cancer (2016) 2, 16026; doi:10.1038/npjbcancer.2016.26; published online 24 August 2016 INTRODUCTION 2010 Dietary Guidelines for Americans and has been found to be a valid and reliable measure of diet quality. Though research to With advances in early detection and treatment, the 5-year date is limited, existing studies suggest that higher diet quality is survival rate for breast cancer has increased to almost 90% for all stages combined. Yet despite these gains, breast cancer remains not associated with breast cancer mortality, but is associated with a the second leading cause of cancer deaths among US women. reduction in deaths from non-breast cancer causes among breast 12–14 Among breast cancer survivors, obesity at diagnosis is associated cancer survivors. While some previous studies have assessed with an increased risk of disease recurrence and both all-cause post-intervention changes in dietary components among breast 15–22 and breast cancer-specific mortality. Weight gain post diagnosis cancer survivors, few have evaluated changes in overall diet 4–6 23,24 may also be associated with a poor prognosis. The majority of quality. This is an important area to explore, as changes in diet breast cancer patients gain weight while undergoing treatment, quality may be independently associated with improvements in and many continue to gain weight in the years following the long-term health of breast cancer survivors. diagnosis. Breast cancer survivors are also at an increased risk The Lifestyle, Exercise, and Nutrition (LEAN) study was a of cardiovascular disease and diabetes relative to the general randomized controlled trial of a 6-month weight loss intervention population, both conditions related to being overweight or 25 among overweight and obese breast cancer survivors. Modeled obese. Weight loss and/or weight maintenance is thus an 26 after the successful Diabetes Prevention Program (DPP), the important goal for women following breast cancer diagnosis. LEAN intervention consisted of a series of either in-person or A recent systematic review documented the feasibility and telephone-based counseling sessions that encouraged weight loss effectiveness of comprehensive weight loss interventions for 9 through both physical activity and achieving or maintaining a breast cancer survivors. Although successful interventions have healthy diet. For the primary outcome, participants randomized to included a dietary component, it is unclear whether weight loss is the LEAN intervention achieved significantly greater weight loss accompanied by improvements in diet quality or simply a decrease than those assigned to a control group (6.4% vs 2.0%), as has been in caloric intake and increase in energy expenditure. A focus on reported previously. In this report, we present change in diet diet quality, as opposed to individual foods and nutrients, accounts quality and specific dietary components over the 6-month LEAN for the potentially synergistic effects of foods and food patterns on study in the intervention group compared with the control group. health. The Healthy Eating Index 2010 (HEI-2010) aligns with the 1 2 Department of Chronic Disease Epidemiology, Yale School of Public Health, New Haven, CT, USA; Office of Disease Prevention, National Institutes of Health, Bethesda, MD, USA; 3 4 Department of Internal Medicine, Yale Cancer Center, New Haven, CT, USA and Yale School of Medicine, New Haven, CT, USA. Correspondence: B Cartmel (brenda.cartmel@yale.edu) Received 11 February 2016; revised 10 June 2016; accepted 21 July 2016 Published in partnership with the Breast Cancer Research Foundation Diet quality changes in breast cancer survivors C Anderson et al RESULTS Table 1. Baseline participant characteristics Baseline characteristics by intervention group are presented in Table 1. In both the usual care and intervention groups, the Usual care Intervention P value majority of participants were white, married, postmenopausal, and (n = 30) n (%) (n = 51) n (%) well-educated. Baseline characteristics were similar between the Age (mean± s.d.) 57.90± 7.41 59.24± 7.15 0.426 intervention and the usual care groups with the exception of BMI (mean± s.d.) 33.99± 7.84 32.78± 6.40 0.453 alcohol intake, which was significantly higher in the intervention White 27 (90.0) 47 (94.0) 0.667 group (Po0.008). Over the 6-month intervention, average Latino 0 (0.0) 2 (3.9) 0.528 percentage of body weight lost was 6.4% in the intervention College graduate 20 (66.7) 35 (68.6) 0.855 group and 2.0% in the usual care group (Po0.01). Currently married 17 (56.7) 34 (66.7) 0.368 Table 2 shows the average HEI score and individual dietary Postmenopausal 23 (76.7) 42 (82.4) 0.535 Ever smoker 13 (43.3) 20 (39.2) 0.716 components by group at baseline and 6 months. At baseline, the Drink alcohol 23 (76.7) 48 (96.0) 0.008 average HEI score was 70.17 (s.d. = 8.51) in the intervention group 1st degree family 9 (30.0) 16 (32.0) 0.852 and 71.08 (s.d. = 9.27) in the usual care group (P=0.788). At history of breast cancer 6 months, the HEI score improved by 6.80 (s.d. = 10.06) in the Stage 0.946 intervention group. This was nearly double the 3.05 (s.d. = 8.03) 0 6 (20.0) 8 (15.7) increase in the usual care group, though the difference in change in I 15 (50.0) 26 (51.0) HEI score between groups was not statistically significant (P=0.09). II 6 (20.0) 13 (25.5) Significant differences between groups were observed for III 2 (6.7) 3 (5.9) Unknown 1 (3.3) 1 (2.0) change over the 6-month study for four of the eight diet Treatment 0.868 components targeted by our intervention (Table 2). Relative to the Neither chemo nor 5 (16.7) 7 (13.7) usual care group, the intervention group reported greater radiation reductions in percent energy from total fat and from saturated Radiation only 12 (40.0) 17 (33.3) fat. Specifically, percent energy from total fat decreased by 4.19% Chemo only 4 (13.3) 9 (17.7) (s.d. = 6.49) in the intervention group, as compared with a 1.12% Both radiation and 9 (30.0) 18 (35.3) (s.d. = 6.72) reduction in the usual care group (P = 0.01). Percent chemo energy from saturated fat decreased by 2.20% (s.d. = 2.39) in the Current endocrine 24 (82.8) 40 (83.3) 0.948 therapy intervention group and by 1.05% (s.d. = 2.16) in the usual care group (P = 0.003). The intervention group also reported greater a 2 T-tests for continuous variables and χ -test for categorical variables. increases in fiber intake and fruit servings at 6 months. Fiber grams increased by 4.84 g per 1,000 kcal (s.d. = 4.72) among the intervention group and 1.28 g per 1,000 kcal (s.d. = 4.21) among frequently assessed in weight loss intervention studies. The HEI the usual care group (P = 0.007). Fruit servings increased by 0.66 emphasizes consumption of more fruits, vegetables, and whole servings (s.d. = 1.66) in the intervention group and decreased by grains and less refined grains, sodium, and empty calories. High 0.37 servings (s.d. = 1.51) in the usual care group (P = 0.006). For scores on the HEI reflect diets with an appropriate balance of food the remaining dietary intake variables—including calories, fat groups, rather than individual nutrients, thus allowing for the grams, added sugar, and vegetables servings—the intervention potentially synergistic effects of individual dietary components to group improved to a greater extent than the usual care group, but be evaluated. The average HEI score among LEAN participants at differences between groups were not statistically significant. Within group associations between percent weight loss and baseline was ~ 70, comparable to that found among participants change in HEI score are shown in Table 3. There was a significant who voluntarily enroll in large diet studies, such as the NIH-AARP Diet and Health Study. On the other hand, a recent study using correlation between percent weight loss and change in HEI in data from the National Health and Nutrition Examination Survey the intervention group (r = − 0.42 P = 0.002) with the increase in (NHANES) reported an average HEI-2010 score of only 51 among HEI score greater among participants who lost at least 5% of breast cancer survivors, suggesting that LEAN participants were their initial body weight, relative to those who lost o5% (10.35 vs already eating relatively healthy diets. 2.82, P = 0.01). In the general population, higher scores on the HEI-2010 have been associated with reduced all-cause mortality, as well as DISCUSSION cardiovascular disease and cancer-specific mortality among 31,33,34 This study evaluated the effect of a 6-month lifestyle and weight women. Using the previous version of the HEI, the HEI-2005, loss intervention on diet quality and selected dietary components an inverse association between post-diagnosis diet quality and all- among overweight and obese breast cancer survivors. Results cause mortality has also been documented among breast cancer demonstrate that the LEAN intervention, which resulted in an survivors. However, the relationship between diet quality and average 6.4% weight loss, was successful in increasing fruit and breast cancer-specific survival remains unclear, as few studies have 12–14 fiber consumption and in decreasing percent energy from both fat examined such associations. To our knowledge, the impact of and saturated fat. Though differences between intervention and post-diagnosis changes in diet quality on breast cancer outcomes usual care groups were not significant, changes in diet quality as has also not been explored. At 6 months, participants in the LEAN intervention improved their HEI-2010 score by an average of 6.8 assessed by the HEI-2010 were in the expected direction. Of note, intervention participants who lost more weight had greater points, and those who lost at least 5% of their initial body weight increases in HEI score, suggesting that improvements in overall demonstrated an increase of over 10 points. Further studies are diet quality were an additional benefit of the intervention among needed to evaluate the impact of such changes—both alone and in women who achieved successful weight loss. conjunction with weight loss—on outcomes among breast cancer Previous reports have documented post-intervention changes survivors. in other diet quality indices among survivors of breast cancer and Notably, we also observed significant changes in components 23,24,27–29 other cancer types. However, this report is unique for the of the diet that were specifically emphasized in the structure of focus on change in the HEI-2010, the most recent version of the the LEAN intervention. Decreasing energy intake from fat was HEI, in addition to the change in specific dietary components emphasized as a way to reduce caloric intake and promote weight npj Breast Cancer (2016) 16026 Published in partnership with the Breast Cancer Research Foundation Diet quality changes in breast cancer survivors C Anderson et al Table 2. Comparison of dietary components and HEI-2010 scores between intervention (n= 51) and usual care (n= 30) Baseline (mean ± s.d.) 6 months (mean ± s.d.) Change (mean ± s.d.) P value Calories 0.561 Intervention 1,836.03± 784.92 1,481.07± 466.74 − 354.96± 725.65 Usual care 1,762.25± 747.39 1,522.64± 674.85 − 239.61± 680.25 % Energy from fat 0.013 Intervention 32.22± 8.26 28.03± 6.26 − 4.19± 6.49 Usual care 31.99± 6.92 30.87± 5.76 − 1.12± 6.72 Fat (g) 0.096 Intervention 67.84± 37.40 46.43± 19.84 − 21.41± 34.37 Usual care 64.10± 32.21 52.99± 25.09 − 11.12± 27.93 % energy from saturated fat 0.003 Intervention 10.29± 2.91 8.09± 2.24 − 2.20± 2.39 Usual care 10.34± 2.73 9.29± 1.79 − 1.05± 2.16 Added sugar (gm per 1,000 kcal) 0.084 Intervention 30.04± 15.38 25.14± 10.18 − 4.90± 14.95 Usual care 32.76± 10.72 30.33± 13.47 − 2.44± 9.37 Fiber (gm per 1,000 kcal) 0.007 Intervention 12.22± 3.84 17.06± 4.98 4.84± 4.72 Usual care 12.56± 4.29 13.83± 4.27 1.28± 4.21 Fruit servings 0.006 Intervention 2.18± 1.43 2.84± 1.81 0.66± 1.66 Usual care 2.35± 1.77 1.98± 1.33 − 0.37± 1.51 Vegetable servings 0.106 Intervention 2.79± 1.54 3.32± 1.74 0.53± 1.58 Usual care 2.72± 1.79 2.74± 2.02 0.02± 1.20 HEI-2010 score 0.092 Intervention 70.17± 8.51 76.97± 9.80 6.80± 10.06 Usual care 71.08± 9.27 74.13± 9.09 3.05± 8.03 Abbreviation: HEI, healthy eating index. P value for difference between groups in change in intake (6 months—baseline), controlling for baseline. survivors. Furthermore, the LEAN study was not powered to detect Table 3. Change in HEI score by percentage of weight loss changes in diet quality, as this was not a primary outcome. Larger studies are needed to evaluate the impact of weight loss Weight loss o5% Weight loss ⩾ 5% P value interventions, such as the LEAN intervention, on HEI scores and Intervention 2.82± 7.20 10.35± 11.09 0.010 ultimately the impact of diet quality on recurrence and survival. Usual care 2.38± 8.15 4.89± 7.90 0.268 Even though LEAN participants may have been eating a healthier diet compared with the general population, as evidenced by their Abbreviation: HEI, healthy eating index. relatively high HEI scores at enrollment, we still saw modest P value for difference in change in HEI score by weight loss %, within each group, controlling for baseline HEI score. improvements in the intervention group for HEI score and significant Intervention group: weight loss o5% (n= 23); weight loss ⩾ 5% (n= 27). improvements for diet components targeted by our intervention. Usual care group: weight loss o5% (n= 22); weight loss ⩾5% (n = 8). These dietary changes could be attributed to the fact that women who volunteer for intervention trials are also often more educated and more motivated than a more general population sample. However, a breast cancer diagnosis may represent a teachable loss, while the increases in fruit and fiber consumption were moment, and thus many survivors may be highly motivated to make consistent with the recommendation to eat a predominately lifestyle changes, such as improving their diet. plant-based diet. Though not significantly different from the usual In summary, the efficacious LEAN weight loss intervention care group, other aspects of diet, including intakes of vegetables improved several aspects of diet among breast cancer survivors. and added sugars, also improved in the intervention group compared with the usual care group. While some studies have The changes observed reflect key recommendations of the dietary suggested that diets low in saturated fat and high in fruits and counseling in the intervention. Diet quality also changed favorably vegetables are associated with improved breast cancer prognosis among intervention participants, particularly those who lost a and survival, such associations have not been demonstrated greater percentage of their body weight. These findings suggest 35,36 consistently. However, such diets have been shown to that weight loss interventions can favorably impact participants’ 31,33,34 decrease mortality from heart disease, the most common diet quality, with potential implications for the overall health and cause of death in breast cancer survivors. longevity of breast cancer survivors. Future trials should be Though this study has several strengths, including the designed to assess the impact of dietary change on long-term randomized design and counseling from a registered dietician outcomes such as recurrence and survival. to target dietary changes, there are also potential limitations. One limitation is measurement error inherent to the food frequency MATERIALS AND METHODS questionnaire (FFQ). In addition, the use of an FFQ to assess dietary change may lead to differential reporting between Participants intervention and control groups. LEAN participants were also Women who had a body mass index (BMI)⩾ 25.0 kg/m and had been fairly homogenous with respect to sociodemographic character- diagnosed with Stage 0 to III breast cancer in the 5 years prior to istics such as age and race/ethnicity, and thus our results may not enrollment were eligible for the study. Eligible participants also had be generalizable to other more diverse groups of breast cancer completed chemotherapy and/or radiation and were physically able to Published in partnership with the Breast Cancer Research Foundation npj Breast Cancer (2016) 16026 Diet quality changes in breast cancer survivors C Anderson et al exercise. Women had to be accessible by telephone and be able to read components or 1 ounce (1 ounce = 28.35 g) in the grains or protein foods and communicate in English. Details of recruitment procedures can be components. found elsewhere. Briefly, the study was advertised in the Breast Center at The HEI-2010 is calculated by summing 12 component scores, each of Smilow Cancer Hospital at Yale-New Haven and the Yale Cancer Center which reflects recommendations in the 2010 Dietary Guidelines for Survivorship Clinic. Women self-referred and were recruited between 1 Americans. Component scores are calculated using a density-based June 2011 and 30 December 2012. The study was approved by the Yale approach (i.e., per 1,000 kcal or percent of total energy), and higher scores School of Medicine Human Investigation Committee. for all components reflect closer adherence to the Dietary Guidelines. One One hundred eligible women agreed to randomization and gave component, empty calories (calories from solid fats and added sugars that informed consent. Using a random permuted block design, participants add no nutrients) is scored from 0 to 20. Five components (whole grains, were randomly assigned to one of the following groups: in-person dairy, fatty acids, refined grains, and sodium) are scored from 0 to 10, and counseling, telephone-based counseling, or usual care. Eighty-one women six components (total fruit, whole fruit, total vegetables, greens and beans, (81%), (51 intervention, 30 usual care) had complete dietary data and were total protein foods, and seafood and plant proteins) are scored from 0 to 5. included in the analysis. Components to be consumed in moderation—refined grains, sodium, and empty calories—are reverse scored. Thus the possible range for the total HEI score (the sum of the 12 components) is 0–100. For each participant Intervention groups in the LEAN study, the 12 HEI component scores and a total HEI score were For both the in-person and telephone-based counseling groups, the calculated for both the baseline and 6-month dietary assessments. In intervention consisted of 11 individualized sessions with a registered addition to HEI scores, diet components that were specifically emphasized dietician. The content of the weight loss program was similar for both in the LEAN intervention were also used to evaluate participants’ diet groups, with only the delivery being different (in-person vs telephone quality. These diet components were derived from the FFQ and included counseling). The sessions, ~ 30 min in duration, occurred each week for the calories, percent energy from fat, percent energy from saturated fat, added first month, followed by bimonthly sessions in months 2 and 3 and sugar, fiber, fruit servings, and vegetable servings. monthly sessions in months 4–6. The intervention components were adapted from the DPP, as well as Statistical analysis weight management materials from the American Institute for Cancer Research (AICR), the American Cancer Society, and the National Cancer Due to the similarity of intervention components and weight loss Institute. Dietary recommendations were also drawn from the Dietary outcomes between the in-person and telephone-based counseling Guidelines 2010. The primary goal of the intervention was for participants groups, these two groups were combined for the purposes of these to achieve a weight loss of 10% of initial body weight. A combination of analyses. Characteristics of the usual care group and intervention groups reduced caloric intake, increased physical activity, and behavior therapy was were compared using t-tests for continuous variables and Χ -tests or emphasized, with strategies based on constructs of the Social Cognitive Fisher's exacts tests for categorical variables. Theory. For the diet portion of the intervention, participants set goals for For the HEI score and all dietary intake variables, the main outcome was energy intake in the range of 1,200–2,000 kcal per day (based on baseline changed over the intervention period, which was calculated as the 6- weight) and were advised to limit fat consumption to 25% of total energy month value minus the baseline value. To test for differences in average intake. Other targets included increasing fiber intake to 25 g per day and change between the two groups, generalized linear models were used reducing consumption of added sugars. Eating a largely plant-based diet with adjustment for baseline values. To assess whether a change in HEI was also emphasized, with the recommendations to eat a minimum of five score was associated with weight loss, participants within each group were servings of fruits and vegetables per day, and to reduce portion sizes of categorized by their percentage of weight lost (o5% or ⩾ 5%) over the meat and other animal products. course of the intervention period. Analysis of variance was used to To track their personal intake of various dietary components, such as fat compare the change in HEI score by weight loss percent within each and fiber, women in the intervention groups recorded their daily food group, with adjustment for baseline HEI score. consumption in a log book developed for the study. The women were also asked to weigh themselves weekly at home using a scale provided for them. ACKNOWLEDGMENTS We are indebted to the participants for their dedication and time to the LEAN study. Usual care group This study was supported by the AICR and in part by a grant from the Breast Cancer Research Foundation. Also supported in part by the Yale Cancer Center Support Participants assigned to the usual care group received AICR nutrition and Grant (CCSG) P30 CA016359 and the CTSA Grant Number UL1 TR000142 from the physical activity brochures. They were also referred to the Yale Cancer National Center for Advancing Translational Science (NCATS), a component of the Center Survivorship Clinic, which offers a two-session weight management National Institutes of Health (NIH). The authors assume full responsibility for analyses program. Following study completion at 6 months, participants in the and interpretation of these data. usual care group were offered all educational material provided to participants in the counseling groups, as well as an in-person counseling session. CONTRIBUTIONS M.L.I., B.C., M.H., and L.M.F. conceived and designed the study. M.H. recruited the Assessments subjects, conducted data collection, and delivered the intervention. C.A. conducted Medical history and demographic data were collected via questionnaire at the data analysis. S.M.G. and L.M.F. assisted in the data analysis. C.A., B.C., M.L.I., S.M. baseline. Anthropometric measures, including weight and height, were G., M.H., L.M.F., T.S., and C.A. participated in interpreting the data and writing the assessed by study staff during clinic visits at both baseline and 6 months. manuscript. Dietary intake was assessed at baseline and 6 months using a 120-item FFQ. This instrument was developed for the Women’s Health Initiative (WHI) and has been validated against 4-day food records and 24-h dietary COMPETING INTERESTS recalls. The nutrient database used to analyze the WHI FFQ was derived The authors declare no conflict of interest. from the Nutrition Data Systems for Research, version 2005 (the University 41,42 of Minnesota, Minneapolis, MN, USA). 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Daughters and Mothers Against Breast Cancer article are included in the article’s Creative Commons license, unless indicated (DAMES): main outcomes of a randomized controlled trial of weight loss in otherwise in the credit line; if the material is not included under the Creative Commons overweight mothers with breast cancer and their overweight daughters. Cancer license, users will need to obtain permission from the license holder to reproduce the 120, 2522–2534 (2014). material. To view a copy of this license, visit http://creativecommons.org/licenses/ 25. Harrigan, M. et al. Randomized trial comparing telephone versus in-person weight by/4.0/ loss counseling on body composition and circulating biomarkers in women treated for breast cancer: the lifestyle, exercise, and nutrition (LEAN) study. J. Clin. Oncol. © The Author(s) 2016 34,669–676 (2016). Published in partnership with the Breast Cancer Research Foundation npj Breast Cancer (2016) 16026

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