Abstract
Purpose:
The goal of this education and culinary-based dietary intervention was to increase adherence to a Mediterranean-style, anti-inflammatory dietary pattern in breast cancer survivors (BCS) by promoting consumption of anti-inflammatory foods, herbs, and spices.
Methods:
Overweight and obese, early-stage, BCS were randomized to the Intervention (n=76) or Control (n=77). The six-month intervention included monthly nutrition and cooking workshops, Motivational Interviewing telephone calls and individualized newsletters. Control participants received monthly informational brochures and no navigational services. Dietary intakes were collected via questionnaire and 3-day food records at baseline and 6 months.
Results:
One hundred twenty-five BCS (n=60 I; n=65 C) completed post-testing (81.7%) and were included in analyses. Adherence to Mediterranean diet guidelines significantly increased in the intervention group, but not in the control group (+22.5% vs. +2.7%, P <0.001). Upon further analysis of adherence to individual dietary guidelines, the intervention group significantly improved adherence to only three guidelines: consuming ≥ 3 servings of fish or shellfish/week, reducing red meat intake to <1 serving/day, and limiting consumption of commercial sweets and baked goods to <3 times/week. The intervention arm increased the use of spices and herbs compared to control (+146.2% vs. +33.3%, P <0.001), including significantly more frequent consumption of cinnamon, turmeric, garlic, ginger, black pepper, and rosemary.
Conclusion:
An education and culinary-based intervention in BCS successfully increased adherence to a more Mediterranean-style, anti-inflammatory dietary pattern by increasing consumption of antiinflammatory foods, spices and herbs and decreasing consumption of pro-inflammatory foods.
Keywords: Diet, breast cancer survivor, anti-inflammatory, survivorship, Mediterranean diet
Introduction
Breast cancer survivors (BCS) are the largest number of cancer survivors globally, and it is imperative to identify lifestyle interventions that reduce risk of recurrence and comorbidities in cancer survivorship [1]. Dietary interventions in BCS have primarily targeted weight loss because excess weight and body fat are risk factors for recurrence and comorbidities such as cardiovascular disease and diabetes [2, 3]; however, there is growing evidence that pro-inflammatory dietary patterns may also be a significant risk factor. As reviewed by Zahedi et al., several studies have demonstrated a relationship between a pro-inflammatory diet and increased risk of breast cancer [4]. Additionally, a more anti-inflammatory diet post-breast cancer diagnosis was associated with a reduced risk of cardiovascular disease mortality [5]. Thus, dietary patterns may play an essential role in modifying inflammation and reducing risk of comorbidities and recurrence in BCS.
An example of an anti-inflammatory dietary pattern is the Mediterranean diet which is characterized by high intakes of fruit and vegetables, whole grains, nuts, legumes, fish, monounsaturated fat (olive oil); moderate intakes of dairy products and alcohol; and low intakes of meat and meat products and saturated fat [6]. Adherence to a Mediterranean-type diet has been associated with a multitude of health benefits [7] including lower risk of all-cause mortality [8], cancer [9], type II diabetes [10], cardiovascular disease [11], and cognitive decline [12]. The Mediterranean dietary pattern is high in anti-inflammatory micronutrients and phytochemicals such as n-3 fatty acids, flavonoids, carotenoids, and vitamins C and E, and higher adherence to the Mediterranean has been associated with lower levels of inflammatory markers [13–15]. Thus, greater adherence to a Mediterranean dietary pattern may elicit health benefits through impacts on systemic inflammation [16]. Additionally, Mediterranean-style diets have been demonstrated to elicit cardiovascular benefits including improved endothelial function and reductions in serum cholesterol and triglycerides [17, 18] In a six-month randomized controlled trial, BCS who adhered to a Mediterranean type diet had beneficial changes in body composition, cholesterol, and glucose levels compared to controls [19].
Selecting foods that are anti-inflammatory while avoiding proinflammatory foods may be health protective in BCS. Although many nutrients and foods are suggested to have anti-inflammatory potential, a variety of spices and herbs may also contribute to a diet’s anti-inflammatory and overall health protective role. Culinary spices and herbs contain polyphenols and other antioxidants which are strong antagonists against tumorigenesis, carcinogen bioactivation and inflammation [20–22]; however, these activities have primarily been demonstrated within in vitro and in vivo models, and more human clinical trials are needed.
There are several epidemiological studies associating health benefits with anti-inflammatory foods and dietary patterns in healthy populations, but limited dietary interventions have promoted this dietary pattern in BCS. Furthermore, even fewer have been conducted in diverse populations. The goal of this education and culinary-based dietary intervention was to improve adherence to an anti-inflammatory dietary pattern in BCS by promoting consumption of anti-inflammatory foods, herbs, and spices.
Methods
Study Design and Participants
The randomized controlled trial on which this analysis was based has been previously described [23]. Briefly, we recruited 153 overweight and obese (BMI ≥25 kg/m2), early-stage (0-III), English-speaking breast cancer survivors who had completed treatment at least 2 months prior to study enrollment. Participants were randomized to an Intervention (I; n=76) or Control (C; n=77) arm (Figure I). Measures were obtained at baseline, and repeated at 6 months.
Figure I. CONSORT diagram for randomized, controlled dietary intervention.
Intervention
The Intervention consisted of individualized anti-inflammatory dietary guidelines and behavior-change cues delivered during six monthly in-person Anti-inflammatory (AI) nutrition workshops; monthly Motivational Interviewing (MI) telephone calls by trained, patient navigators; and monthly newsletters tailored to individual change readiness.
The purpose of the AI nutrition workshops was to increase participant knowledge of the relationship between diet and cancer; describe AI foods and how they can help reduce risk for cancer recurrence; and promote behaviors aimed at increasing regular AI food intake. To optimize the intervention experience given limited space and culinary resources, women were grouped into 5 cohorts (10–20/cohort). Each cohort was asked to attend six monthly workshops beginning immediately following randomization. A total of 30 workshops were delivered during the study period.
Each nutrition workshop consisted of a didactic portion with PowerPoint slides, followed by a cooking demonstration with a chef skilled in AI food preparation, a tasting, and interactive discussion among participants, study investigators and staff. Participants received paper copies of lecture slides, a description of the properties and benefit of featured AI foods, and recipes and supply lists for the food demonstration. Workshop attendance was tracked. Participants who missed a workshop session were contacted by a patient navigator and provided with electronic copies of all materials. Table I shows the themes and objectives, AI foods discussed and highlighted, and recipes demonstrated during each workshop.
Table I.
Monthly Workshops
| Workshop | Theme/Objectives | AI Foods featured in lecture | Recipes |
|---|---|---|---|
| 1 | Relationship between cancer, inflammation and diet Become familiar with components of the AI diet. Understand how AI foods can prevent cancer. | Deep Marine Fish (wild) Bright multi-colored vegetables and fruit (red grapes and berries, pomegranate, citrus) Green tea turmeric, ginger, black pepper, chilies, chives, garlic, onion | 1) Zesty Citrus Salad with Ginger 2) Lemon Grouper with Fresh Garden Vegetables |
| 2 | Understand American Cancer Society recommendations to prevent cancer recurrence and spread. Learn how to reduce risk of recurrence or spread by using key food groups in one’s own kitchen. | Alcohol Preserved/cooked meats Soy Turmeric and rosemary Green tea Cruciferous vegetables (collards, mustard greens) | 1) Oven Roasted Oatmeal Crumble with Cranberries 2) Sweet and Spicy Pepita Snack Mix |
| 3 | Exploring nature’s anti-cancer cuisine. Understand AI foods as chemoprevention -- which foods when consumed regularly have an anti-inflammatory effect. | Cruciferous vegetables (broccoli, watercress, cauliflower, Brussels sprouts, rapini, bok choy, kale, cabbage) Canola/rapeseed oil Wasabi, garlic | 1) Savory Broccoli Fritters 2) Asian Slaw with Serrano Chiles |
| 4 | Understand the value of antioxidants and how they fit into the AI diet -- which foods when consumed daily have an antioxidant effect. Learn how to reduce risk of recurrence or spread by consuming more antioxidant–rich foods. | Black pepper Lemongrass Green tea | 1) Refreshing Summer Agua Fresca 2) Green Tea Vinaigrette with Garden Basil |
| 5 | Understand regulations governing supplements and which products have been scientifically proven to work. Understand that supplements may be unnecessary if the diet provides adequate nutrients. Learn about Vitamin D and calcium, and why they are recommended as dietary supplements | Turmeric Smoked salmon/light tuna Whole eggs Vitamin-D fortified milk, yogurt Calcium-fortified bread, orange juice, cereal Spinachcar | 1) Frozen Watermelon and Greek Yogurt Popsicle with Black Pepper and Ginger 2) Breakfast Frittata with Fresh Vegetables and Cheeses |
| 6 | Understand how the objectives of workshops 1–5 work together to impact recurrence risk and prevention of future cancers. Learn how the right type of chocolate can be beneficial in an anti-inflammatory diet. | Chocolate (>75% cacao) | 1) Cardamom Chicken Bites with Cracked Black Pepper Black Bean Dip with Cocoa and Chipotle |
At the end of each workshop, participants received a carbon copy sheet containing 4–6 goals related to workshop content. They were asked to select 1–2 goals to work on over the next month until the following workshop. The sheet also contained importance and confidence scales based on Stages of Change (SOC) [24] and space to identify barriers to making changes as well as strategies to overcome these barriers. Participants turned in one copy to study staff and kept a copy with their other study materials. During follow-up MI telephone calls, patient navigators used the sheets to discuss progress, barriers and strategies with participants, as well as assess their SOC. A new goal sheet was distributed at each workshop, and participants were encouraged to either work on the same goals or select new ones.
Control
Control participants received monthly American Institute for Cancer Research informational brochures, two telephone calls prior to each assessment appointment, and no navigational services.
Dietary Intake
At baseline and 6 months, participants completed questionnaires to assess adherence to the Mediterranean diet [6] and spice and herb consumption [23]. The Mediterranean diet assessment tool consisted of 14 questions that were coded one for an answer in agreement with a Mediterranean diet and zero for nonadherence. Responses were added for a total value between 0 and 14, with higher scores indicating greater adherence. The spices and herbs questionnaire included questions about the frequency of use of 13 different spices and herbs that were the focus of the intervention. Use of the spice or herb 4 or more times per a week was coded as a 1, while less than 4 times a week was scored a zero. The questions were added for a total possible value of 0–13. Participants were also instructed to maintain a detailed 3-day food record (two weekdays and one weekend day) prior to each assessment. Food records were entered in Food Processor ® (ESHA Research, Salem, OR) for nutrient analysis. Missing or incomplete dietary questionnaires or food records were not included in the analyses.
Statistical Analyses
Unadjusted comparisons between groups on baseline demographics measures were conducted using twosample t tests for continuous variables and Χ2-tests or Fisher’s exacts tests for categorical variables. The main outcome was change over the intervention period, which was calculated as the 6 month value minus the baseline value. Differences in average change of Mediterranean diet score, spices and herbs score, and nutrient intakes between groups were assessed using general linear models with adjustment for baseline values. McNemar’s test was used for within-group comparisons of dichotomous variables including adherence to individual Mediterranean diet guidelines and use of individual herbs and spices. Statistical tests used ∝≤0.05 and two-sided p-values. All analyses were performed using SPSS v24.
Results
Demographics
Analyses are based on 125 breast cancer survivors (n=60 intervention; n=65 control) that completed 6 month analyses. There were no statistically significant differences in demographic or clinical characteristics between intervention and control groups (Table II). The combined average age of the sample was 57.0 (SD 9.3). Over half of participants (54.4%) reported a college degree or higher, 45.6% reported working full time, and 74.2% reported a monthly household income of >$2,000. Over half (51.2%) of study participants were Latina. The majority of participants were diagnosed with Stage II or lower (68.0%) and 24 or more months post treatment (63.2%).
Table II.
Sample Characteristics
| Intervention n (%) | Control n (%) | p-value | |
|---|---|---|---|
| Age (Mean ± SD) | 55.3 ± 10.3 | 58.4 ± 8.2 | .083 |
| BMI (Mean ± SD) | 31.2 ± 4.1 | 32.7 ± 5.2 | .066 |
| Ethnicity | .984 | ||
| Anglo | 25(41.7) | 28(43.1) | |
| Latino | 31(51.7) | 33(50.8) | |
| Other | 4(6.7) | 4(6.2) | |
| Education | .127 | ||
| High school graduate or less | 9(15.0) | 7(10.8) | |
| Some college/Assoc. degree | 24(40.0) | 17(26.2) | |
| College graduate or higher | 27(45.0) | 41(63.1) | |
| Employment Status | .100 | ||
| Full Time | 30(50.0) | 27(41.5) | |
| Part Time | 5(8.3) | 8(12.3) | |
| Unemployed Student | 21(35.0) 4(6.7) | 30(46.2) 0(0.0) | |
| Marital Status | .577 | ||
| Married/Cohabitating | 43(71.7) | 42(64.6) | |
| Divorced/widowed/separated | 11(18.3) | 17(26.2) | |
| Single | 6(10.0) | 6(9.2) | |
| Household Monthly Income | .752 | ||
| Under $1500 | 4(6.7) | 6(9.4) | |
| $1500-$2000 | 7(11.7) | 11(17.2) | |
| Over $2000 | 48(78.3) | 45(70.3) | |
| Time Since Last Treatment | .948 | ||
| Less than 6 months | 8(13.3) | 8(12.3) | |
| 6 months | 4(6.7) | 4(6.2) | |
| 12 months | 5(8.3) | 6(9.2) | |
| 18 months | 4(6.7) | 7(10.8) | |
| ≥ 24 months | 40(65.0) | 40(61.5) | |
| Stage of Cancer | .824 | ||
| Stage 0 | 5(8.3) | 7(10.8) | |
| Stage 1 | 18(30.0) | 17(26.2) | |
| Stage 2 | 20(33.3) | 18(27.7) | |
| Stage 3 | 8(13.3) | 13(20.0) | |
| Don’t Know | 9(15.0) | 10(15.4) | |
| Treatment Type | |||
| Surgery | 57(95.0) | 60(92.3) | .539 |
| Chemotherapy | 37(61.7) | 45(69.2) | .374 |
| Radiation | 38(63.3) | 39(60.0) | .702 |
| Hormonal Therapy | 16(26.7) | 26(40.0) | .115 |
| Antibody Therapy | 6(10.0) | 7(10.8) | .888 |
| Reconstruction | 23(38.3) | 25(38.5) | .988 |
Totals may not equal 100% due to missing/refused.
Mediterranean Diet Adherence
Adherence to Mediterranean dietary guidelines at baseline and 6 months is shown in Table IV. Overall at baseline, there was low adherence to Mediterranean dietary guidelines in both groups. Adherence to Mediterranean diet guidelines significantly increased in the intervention group, but not in the control group (+1.6 vs. +.2, P <0.001). When further examining adherence to individual guidelines, the intervention group significantly improved adherence to three guidelines (Table III). At 6 months 86.4% of the intervention group reported consuming less than one serving of red meat a day, which was significantly higher than the 64.4% adherence at baseline (P =0.002). At baseline, 13.6% of the intervention group reported consuming 3 or more servings of fish or shellfish week, which increased to 35.6% at 6 months (P =0.002). Additionally, 86.4% reported limiting consumption of commercial sweets and pastries to less than 3 times a week compared to only 69.5% at baseline (P =0.01).
Table IV.
Comparison of Mediterranean Diet and Spices and Herbs scores between intervention and control
| Baseline | 6 months | Change | P-value a | |
|---|---|---|---|---|
| Mediterranean Diet Score | <.001 | |||
| Intervention | 7.1 (0.3) | 8.7 (0.3) | +1.6 (0.2) | |
| Control | 7.4 (0.3) | 7.6 (0.3) | +0.2 (0.2) | |
| Spices and Herbs Score | <0.001 | |||
| Intervention | 1.3 (0.2) | 3.2 (0.3) | +1.9 (0.3) | |
| Control | 1.2 (0.1) | 1.6 (0.3) | +0.4 (0.2) |
Values are Estimated Marginal Means ± SE
P value for difference between groups in change in intake controlling for baseline
Table III.
Adherence to Individual Mediterranean Diet Guidelines
| Intervention | Control | |||||
|---|---|---|---|---|---|---|
| Baseline (%) | 6 Months (%) | Withingroup difference, p | Baseline (%) | 6 Months (%) | Withingroup differenc e, p | |
| Do you use olive oil or canola oil as a main culinary fat? (yes) | 94.9 | 100.0 | 0.25 | 87.7 | 86.2 | 1.00 |
| How much olive oil or canola oil do you consume in a given day? (>4T/day) | 13.8 | 19.0 | 0.61 | 15.4 | 15.4 | 1.00 |
| How many vegetable servings do you consume per day? (≥2 servings/day) | 54.2 | 64.4 | 0.21 | 52.3 | 64.6 | 0.12 |
| How many fruit units do you consume per day? (≥3 servings/day) | 30.5 | 40.7 | 0.18 | 25.0 | 31.3 | 0.42 |
| How many servings of red meat, hamburger or meat products do you consume per day? (<1 serving/day) | 64.4 | 86.4 | .002 | 78.1 | 78.1 | 1.00 |
| How many servings of butter, margarine, or cream do you consume per day? (<1 serving/day) | 59.3 | 74.6 | 0.07 | 76.2 | 63.5 | 0.08 |
| How many sweet or carbonated beverages do you drink per day? (<1/day) | 74.6 | 86.4 | 0.07 | 68.8 | 76.6 | 0.23 |
| How many glasses of wine do you drink per week? (≥7 glasses/week) | 5.1 | 0.0 | 0.25 | 7.9 | 11.1 | 0.69 |
| How many servings of legumes do you consume per week? (≥3 servings/week) | 33.9 | 45.8 | 0.17 | 23.4 | 34.4 | 0.12 |
| How many servings of fish or shellfish do you consume per week? (≥3 servings/week) | 13.6 | 35.6 | .002 | 25.0 | 21.9 | 0.75 |
| How many times per week do you consume commercial sweets or pastries (not homemade), such as cakes, cookies, biscuits or custard? (<3 times/week) | 69.5 | 86.4 | 0.01 | 69.8 | 76.2 | 0.22 |
| How many servings of nuts do you consume per week? (≥3 servings/week) | 44.8 | 56.9 | 0.17 | 53.1 | 50.0 | .82 |
| Do you preferentially consume chicken or turkey meat instead of pork, hamburgers or sausage? (yes) | 86.4 | 93.2 | 0.13 | 85.9 | 87.5 | 1.00 |
| How many times per week do you consume vegetables, pasta, rice or other dishes seasoned with tomato, onion, leek, garlic and simmered with olive oil? (≥2 times/week) | 61.0 | 78.0 | 0.06 | 64.1 | 60.9 | 0.83 |
Spices and Herbs Intake
At month 6, the intervention arm compared to controls reported an increase in the use of spices and herbs (+1.9 vs. +.4, P <0.001) (Table IV). Compared to baseline, the intervention arm significantly increased the use of cinnamon, turmeric, garlic, ginger, black pepper, and rosemary; however, no significant increase in the use of cardamom, black cumin, cloves, oregano, lemongrass, chives, and thyme was observed (Table VI). The control arm only significantly increased the use of cinnamon.
Table VI.
Change in Use of Individual Spices and Herb
| Intervention | Control | |||||
|---|---|---|---|---|---|---|
| Used spice ≥ 4 times/week | Baseline (%) | 6 Months (%) | Withingroup difference, p | Baseline (%) | 6 Months (%) | Withingroup difference, p |
| Cinnamon | 15.2 | 35.6 | .002 | 9.5 | 2.6 | .039 |
| Cardamom | 1.7 | 6.8 | .375 | 1.6 | 0.0 | 1.00 |
| Turmeric | 8.5 | 22.0 | .021 | 6.3 | 4.8 | 1.00 |
| Garlic | 39.0 | 69.5 | <.001 | 32.8 | 42.2 | .180 |
| Ginger | 0.0 | 31.6 | <.001 | 3.1 | 6.3 | .625 |
| Black Pepper | 54.2 | 84.7 | <.001 | 54.7 | 65.6 | .167 |
| Cumin | 1.7 | 11.9 | .070 | 3.1 | 4.7 | 1.00 |
| Rosemary | 1.7 | 16.9 | .004 | 0.0 | 1.6 | 1.00 |
| Cloves | 0.0 | 3.4 | .500 | 0.0 | 1.6 | 1.00 |
| Oregano | 1.7 | 8.5 | .219 | 1.6 | 3.1 | 1.00 |
| Lemongrass | 0.0 | 1.7 | 1.00 | 3.1 | 3.1 | 1.00 |
| Chives | 0.0 | 6.8 | .125 | 4.7 | 6.3 | 1.00 |
| Thyme | 0.0 | 8.5 | .063 | 0.0 | 4.7 | .250 |
Nutrient Analysis
Compared to the control group, the intervention group reported a significant reduction in Calorie intake (−195.5 vs. +34.8, P=0.045) (Table V). Changes from baseline in percent Calories from fat, percent Calories from carbohydrates, percent Calories from protein, percent Calories from saturated fat, sodium, fiber, fruit servings, and vegetable servings were not statistically significant between groups.
Table V.
Dietary Changes Between Baseline and 6 Month
| Baseline | 6 Months | Change | P value a | |
|---|---|---|---|---|
| Calories | .045 | |||
| Intervention | 1779.3 (92.2) | 1578.3 (85.6) | −195.5 (83.0) | |
| Control | 1765.8 (85.0) | 1805.3 (79.0) | +34.8 (76.6) | |
| % Calories from fat | .815 | |||
| Intervention | 34.5 (1.1) | 35.7 (1.2) | +0.6 | |
| Control | 36.6 (1.0) | 36.3 (1.1) | +0.3 | |
| % Calories from saturated fat | .164 | |||
| Intervention | 10.3 (.5) | 11.2 (0.5) | +0.6 | |
| Control | 11.5 (.5) | 10.9 (0.5) | −0.4 | |
| % Calories from protein | .634 | |||
| Intervention | 17.3 (0.6) | 18.8 (0.8) | +1.4 (0.8) | |
| Control | 17.3 (0.6) | 18.2 (0.7) | +0.9 (0.7) | |
| % Calories from carbohydrates | .954 | |||
| Intervention | 48.2 (1.4) | 45.7 (1.4) | −1.5 (1.4) | |
| Control | 45.5 (1.3) | 44.9 (1.3) | −1.4 (1.3) | |
| Fiber (g) | .616 | |||
| Intervention | 10.2 (1.8) | 9.1 (1.7) | −1.8 (1.3) | |
| Control | 13.5 (1.6) | 11.9 (1.6) | −0.9 (1.2) | |
| Sodium (mg) | .674 | |||
| Intervention | 2464.3 (142.7) | 2370.7 (133.4) | −105.0 (131.3) | |
| Control | 2490.6 (131.6) | 2451.3 (123.1) | −29.6 (121.1) | |
| Fruit (cups) | .601 | |||
| Intervention | 1.1 (.2) | 1.0 (0.1) | −0.2 (.1) | |
| Control | 1.2 (.2) | 0.9 (0.1) | −0.3 (.1) | |
| Vegetable (cups) | .768 | |||
| Intervention | 1.6 (.1) | 1.6 (.2) | −.1 (.2) | |
| Control | 1.8 (.1) | 1.7 (.2) | −.1 (.2) |
Values are Estimated Marginal Means ± SE
P value for difference between groups in change in intake controlling for baseline
Discussion
The dietary intervention increased adherence to an anti-inflammatory dietary pattern as demonstrated by increased adherence to Mediterranean diet guidelines and increased use of anti-inflammatory spices and herbs. The Mediterranean diet has shown protection against diseases associated with low-grade inflammation, including cancer, diabetes, obesity, atherosclerosis, metabolic syndrome and cognitive disorders [7, 9–12]. At baseline, both groups had low adherence to Mediterranean dietary guidelines. The Mediterranean diet score significantly increased in the intervention group, but further examination suggested this was largely due to significant increases in adherence to only three specific guidelines: increase of fish consumption, reduction of red meat intake, and limiting consumption of commercial sweets and baked goods. Adherence to a new dietary pattern requires multiple dietary behavior changes compared to interventions that target a specific food group or nutrient. Six months may not be sufficient time for participants to make an impactful change on multiple components. The dietary behaviors that did significantly change were all goals introduced to the intervention group at the beginning of the study, suggesting that these dietary changes required significant time and support.
Although adherence to only three of fourteen guidelines significantly increased, these dietary changes can have significant long-term impacts on health. Most fish are a good source of the omega-3 polyunsaturated fatty acids eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), which have been demonstrated to have anti-inflammatory and anti-carcinogenic properties [25, 26]. Red meat was classified as “probably carcinogenic to humans” by the International Agency for Research on Cancer in 2015[27], and the American Institute for Cancer Research cancer prevention guidelines recommends limiting consumption of red meat [28]. Limiting the intake of sweets and baked goods not prepared at home means BCS in the intervention group reduced intake of processed and packaged foods that are typically high in added sugar, sodium and fat. Even though calorie reduction was not a focus of this study, the intervention arm significantly reduced calorie intake. This may have been due to an overall increased adherence to a Mediterranean type diet consisting of less frequent consumption of higher calorie red meat, sweets, and baked goods. However, this reduction in caloric intake did not result in significantly greater weight changes compared to the control group (−.43 vs. +0.14 lbs, P =.619).
Interestingly, despite the discussion of fruits and vegetables at every workshop, intakes of these food groups did not significantly change. Across groups, average consumption of fruits and vegetables was less than 3 servings a day at both baseline and 6 months. This supports a previous report that only 1419% of most cancer survivors meet the recommendation of consuming 5 or more servings of fruits and vegetables per day [29]. Also of note is that at 6 months, none of the participants in the intervention group reported consuming seven or more glasses of wine a week. The Mediterranean diet includes wine consumption, and research suggests moderate wine consumption is associated with health benefits such as lower inflammation and reduced risk of cardiovascular disease [30–32]. Although wine is an abundant source of polyphenols that have anti-oxidant functions [32], alcohol intake may not be appropriate to include as a dietary goal for BCS. Due to the growing research that alcohol consumption is a risk factor for multiple cancers including breast cancer [28], cancer survivors may choose to limit their overall alcohol intake. Future dietary interventions should consider promoting non-alcoholic beverages that are abundant in anti-inflammatory polyphenols such as tea and coffee.
All spices and herbs recommended in this study were chosen for the beneficial health compounds they contained. For example, cinnamon contains multiple bioactive compounds, including polyphenols and cinnamaldehyde, which have been demonstrated to have anti-tumor properties and anti-inflammatory effects [33]. Aside from anti-inflammatory, anticarcinogenic, antimicrobial, and antioxidant properties, some spices and herbs may impact lipid metabolism, stimulate digestion, and have antidiabetic functions [20–22]. The intervention promoted incorporation of spices and herbs in cooking, and resulted in significant increases in the use of cinnamon, garlic, ginger, black pepper, and rosemary. Further investigation is needed to identify potential barriers to increasing consumption of the other herbs and spices such as cardamom, lemongrass, and clove such as cost, availability, or taste preferences.
Several interventions in BCS have successfully changed dietary behaviors such as increasing fruit and vegetables and reducing fat intake [34–38]. Effective interventions incorporated individualized counseling from a registered dietitian or health counselor, individualized progress reports, personalized workbooks, nutritional education, and group support, supporting the need to provide education in combination with personalized support and follow-up. Our intervention utilized multiple strategies including detailed workshops with goalsetting, culinary instruction and recipe booklets to improve cooking skills, and follow-up monthly newsletters and motivational interviewing. Educational group workshops in combination with individual counseling requires significant time and money. Before implementation and dissemination of the dietary intervention in larger samples, further research is needed to identify the components of the intervention that led to successful dietary changes.
The study had several strengths including a moderate sample size with low attrition rates (18.3% lost to follow-up). Additionally, the sample was diverse, consisting of over 50% Latinas. Disparities between non-Latina Whites and Latina breast cancer survivors are evidenced by the lower 5-year survival rates and greater likelihood of risk of recurrence in Latinas [39, 40]. The two largest dietary intervention studies conducted in breast cancer survivors, Women’s Healthy Eating and Living (WHEL) and Women’s Intervention Nutrition Study (WINS) [35, 36], included less than 6% Hispanics in the study, which is not representative of the large and growing population of Latina breast cancer survivors. To our knowledge, only one dietary intervention has been conducted in a Latina breast cancer sample [34, 41]; therefore, our successful dietary intervention in this population addresses an important gap in the current literature.
A limitation of the study was that all assessments of dietary intake were based on self-report. Additionally, there was high incidence of missing data in the food records, reducing the ability to identify changes in individual nutrients. Future studies should consider using nutrient biomarkers to objectively measure changes in dietary intakes. The intervention was only six months; therefore, it is unknown if the educational workshops resulted in long-term dietary changes. Finally, the biological impact of dietary changes were not evaluated. Further research is warranted to evaluate the longitudinal and biological effects of anti-inflammatory dietary changes in BCS, especially among diverse populations.
Overall, the study demonstrated that an education and culinary-based intervention in BCS was successful at increasing adherence to a more anti-inflammatory dietary pattern by increasing consumption of anti-inflammatory foods, spices and herbs and decreasing consumption of pro-inflammatory foods. Dietary patterns are multidimensional, and nutrients and phytochemicals from a variety of foods, spices, and herbs can reduce inflammation through additive or synergistic interactions. Promoting a dietary pattern rather than a specific food good or nutrient may have greater health benefits, but future interventions must identify strategies that enable individuals to successfully change multiple dietary behaviors.
Acknowledgements:
Iverson Brownell for creating and conducting cooking demonstrations for intervention participants and providing input on AI ingredients for participant recipe book.
Funding: This research was supported by Susan G. Komen (SAB08–0005); Redes en Accion: The National Latino Cancer Research Network (U54CA153511); the Institute for Health Promotion Research at UT Health San Antonio; and the UT Health San Antonio Mays Cancer Center through the NCI Cancer Center Support Grant (P30 CA054174).
Footnotes
Conflict of Interest: The authors declare that they have no conflict of interest.
Data Availability: The datasets during and/or analyzed during the current study are available from the corresponding author on reasonable request
Ethical approval: All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments.
REFERENCES
- 1.Miller KD, Siegel RL, Lin CC, et al. (2016) Cancer treatment and survivorship statistics, 2016. CA Cancer J Clin 66:271–289. doi: 10.3322/caac.21349 [DOI] [PubMed] [Google Scholar]
- 2.Reeves MM, Terranova CO, Eakin EG, Demark-Wahnefried W (2014) Weight loss intervention trials in women with breast cancer: a systematic review. Obes Rev 15:749–768. doi: 10.1111/obr.12190 [DOI] [PubMed] [Google Scholar]
- 3.Playdon M, Thomas G, Sanft T, et al. (2013) Weight Loss Intervention for Breast Cancer Survivors: A Systematic Review. Curr Breast Cancer Rep 5:222–246. doi: 10.1007/s12609-0130113-0 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Zahedi H, Djalalinia S, Sadeghi O, et al. (2018) Dietary inflammatory potential score and risk of breast cancer: systematic review and meta-analysis. Clin Breast Cancer. doi: 10.1016/j.clbc.2018.01.007 [DOI] [PubMed] [Google Scholar]
- 5.Zheng J, Tabung FK, Zhang J, et al. (2018) Association between post-cancer diagnosis dietary Inflammatory Potential and Mortality among invasive breast cancer survivors in the women’s health initiative. Cancer Epidemiol Biomarkers Prev 27:454–463. doi: 10.1158/1055-9965.EPI-170569 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Martínez-González MA, Fernández-Jarne E, Serrano-Martínez M, et al. (2004) Development of a short dietary intake questionnaire for the quantitative estimation of adherence to a cardioprotective Mediterranean diet. Eur J Clin Nutr 58:1550–1552. doi: 10.1038/sj.ejcn.1602004 [DOI] [PubMed] [Google Scholar]
- 7.Dinu M, Pagliai G, Casini A, Sofi F (2018) Mediterranean diet and multiple health outcomes: an umbrella review of meta-analyses of observational studies and randomised trials. Eur J Clin Nutr 72:30–43. doi: 10.1038/ejcn.2017.58 [DOI] [PubMed] [Google Scholar]
- 8.Sofi F, Macchi C, Abbate R, et al. (2014) Mediterranean diet and health status: an updated metaanalysis and a proposal for a literature-based adherence score. Public Health Nutr 17:2769–2782. doi: 10.1017/S1368980013003169 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Schwingshackl L, Schwedhelm C, Galbete C, Hoffmann G (2017) Adherence to Mediterranean diet and risk of cancer: an updated systematic review and meta-analysis. Nutrients 9:pii: E1063. doi: 10.3390/nu9101063 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Jannasch F, Kröger J, Schulze MB (2017) Dietary patterns and type 2 diabetes: a systematic literature review and meta-analysis of prospective studies. J Nutr 147:1174–1182. doi: 10.3945/jn.116.242552 [DOI] [PubMed] [Google Scholar]
- 11.Shen J, Wilmot KA, Ghasemzadeh N, et al. (2015) Mediterranean dietary patterns and cardiovascular health. Annu Rev Nutr 35:425–449. doi: 10.1146/annurev-nutr-011215-025104 [DOI] [PubMed] [Google Scholar]
- 12.Lourida I, Soni M, Thompson-Coon J, et al. (2013) Mediterranean diet, cognitive function, and dementia. Epidemiology 24:479–489. doi: 10.1097/EDE.0b013e3182944410 [DOI] [PubMed] [Google Scholar]
- 13.Sureda A, Bibiloni M, Julibert A, et al. (2018) Adherence to the mediterranean diet and inflammatory markers. Nutrients 10:62. doi: 10.3390/nu10010062 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Mayr HL, Tierney AC, Thomas CJ, et al. (2018) Mediterranean-type diets and inflammatory markers in patients with coronary heart disease: a systematic review and meta-analysis. Nutr Res 50:10–24. doi: 10.1016/j.nutres.2017.10.014 [DOI] [PubMed] [Google Scholar]
- 15.Lahoz C, Castillo E, Mostaza J, et al. (2018) Relationship of the adherence to a mediterranean diet and its main components with CRP levels in the Spanish population. Nutrients 10:379. doi: 10.3390/nu10030379 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Casas R, Sacanella E, Estruch R (2014) The immune protective effect of the Mediterranean diet against chronic low-grade inflammatory diseases. Endocr Metab Immune Disord Drug Targets 14:245–54. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Esposito K, Marfella R, Ciotola M, et al. (2004) Effect of a Mediterranean-Style Diet on Endothelial Dysfunction and Markers of Vascular Inflammation in the Metabolic Syndrome. JAMA 292:1440. doi: 10.1001/jama.292.12.1440 [DOI] [PubMed] [Google Scholar]
- 18.Vincent-Baudry S, Defoort C, Gerber M, et al. (2005) The Medi-RIVAGE study: reduction of cardiovascular disease risk factors after a 3-mo intervention with a Mediterranean-type diet or a low-fat diet. Am J Clin Nutr 82:964–971. doi: 10.1093/ajcn/82.5.964 [DOI] [PubMed] [Google Scholar]
- 19.Skouroliakou M, Grosomanidis D, Massara P, et al. (2017) Serum antioxidant capacity, biochemical profile and body composition of breast cancer survivors in a randomized Mediterranean dietary intervention study. Eur J Nutr. doi: 10.1007/s00394-017-1489-9 [DOI] [PubMed] [Google Scholar]
- 20.Kaefer CM, Milner JA (2008) The role of herbs and spices in cancer prevention. J Nutr Biochem 19:347–361. doi: 10.1016/j.jnutbio.2007.11.003 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Srinivasan K (2014) Antioxidant potential of spices and their active constituents. Crit Rev Food Sci Nutr 54:352–372. doi: 10.1080/10408398.2011.585525 [DOI] [PubMed] [Google Scholar]
- 22.Rubió L, Motilva M-J, Romero M-P (2013) Recent advances in biologically active compounds in herbs and spices: a review of the most effective antioxidant and anti-inflammatory active principles. Crit Rev Food Sci Nutr 53:943–953. doi: 10.1080/10408398.2011.574802 [DOI] [PubMed] [Google Scholar]
- 23.Ramirez AG, Parma DL, Muñoz E, et al. (2017) An anti-inflammatory dietary intervention to reduce breast cancer recurrence risk: Study design and baseline data. Contemp Clin Trials 57:1–7. doi: 10.1016/j.cct.2017.03.009 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Bandura A (2004) Health promotion by social cognitive means. Heal Educ Behav 31:143–164. doi: 10.1177/1090198104263660 [DOI] [PubMed] [Google Scholar]
- 25.Calder PC (2010) Omega-3 fatty acids and inflammatory processes. Nutrients 2:355–74. doi: 10.3390/nu2030355 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Gerber M (2012) Omega-3 fatty acids and cancers: a systematic update review of epidemiological studies. Br J Nutr 107:S228–S239. doi: 10.1017/S0007114512001614 [DOI] [PubMed] [Google Scholar]
- 27.Bouvard V, Loomis D, Guyton KZ, et al. (2015) Carcinogenicity of consumption of red and processed meat. Lancet Oncol 16:1599–1600. doi: 10.1016/S1470-2045(15)00444-1 [DOI] [PubMed] [Google Scholar]
- 28.Word Cancer Research Fund/American Institute for Cancer Research (2018) Diet, Nutrition, Physical Activity and Cancer: a Global Perspective. Continuous Update Project Expert Report 2018. [Google Scholar]
- 29.Blanchard CM, Courneya KS, Stein K (2008) Cancer survivors’ adherence to lifestyle behavior recommendations and associations with health-related quality of life: Results from the American Cancer Society’s SCS-II. J Clin Oncol 26:2198–2204. doi: 10.1200/JCO.2007.14.6217 [DOI] [PubMed] [Google Scholar]
- 30.Fragopoulou E, Choleva M, Antonopoulou S, Demopoulos CA (2018) Wine and its metabolic effects. A comprehensive review of clinical trials. Metabolism 83:102–119. doi: 10.1016/J.METABOL.2018.01.024 [DOI] [PubMed] [Google Scholar]
- 31.Artero A, Artero A, Tarín JJ, Cano A (2015) The impact of moderate wine consumption on health. Maturitas 80:3–13. doi: 10.1016/J.MATURITAS.2014.09.007 [DOI] [PubMed] [Google Scholar]
- 32.Rodrigo R, Miranda A, Vergara L (2011) Modulation of endogenous antioxidant system by wine polyphenols in human disease. Clin Chim Acta 412:410–424. doi: 10.1016/J.CCA.2010.11.034 [DOI] [PubMed] [Google Scholar]
- 33.Ribeiro-Santos R, Andrade M, Madella D, et al. (2017) Revisiting an ancient spice with medicinal purposes: Cinnamon. Trends Food Sci Technol 62:154–169. doi: 10.1016/J.TIFS.2017.02.011 [DOI] [Google Scholar]
- 34.Greenlee H, Gaffney A, Aycinena C, et al. (2015) ¡Cocinar Para Su Salud!: Randomized controlled trial of a culturally-based dietary intervention among Hispanic breast cancer survivors. J Acad Nutr Diet 115:709–723. doi: 10.1002/cncr.10244 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 35.Chlebowski RT, Blackburn GL, Thomson CA, et al. (2006) Dietary fat reduction and breast cancer outcome: interim efficacy results From the women’s intervention nutrition study. JNCI J Natl Cancer Inst 98:1767–1776. doi: 10.1093/jnci/djj494 [DOI] [PubMed] [Google Scholar]
- 36.Pierce JP, Natarajan L, Caan BJ, et al. (2007) Influence of a diet very high in vegetables, fruit, and fiber and low in fat on prognosis following treatment for breast cancer: the Women’s Healthy Eating and Living (WHEL) randomized trial. JAMA 298:289–98. doi: 10.1001/jama.298.3.289 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37.Park CL, Cho D, Salner AL, Dornelas E (2016) A randomized controlled trial of two mail-based lifestyle interventions for breast cancer survivors. Support Care Cancer 24:3037–46. doi: 10.1007/s00520-016-3129-y [DOI] [PMC free article] [PubMed] [Google Scholar]
- 38.Demark-Wahnefried W, Clipp EC, Lipkus IM, et al. (2007) Main outcomes of the FRESH START trial: a sequentially tailored, diet and exercise mailed print intervention among breast and prostate cancer survivors. J Clin Oncol 25:2709–2718. doi: 10.1200/JCO.2007.10.7094 [DOI] [PubMed] [Google Scholar]
- 39.American Cancer Society (2015) Cancer Facts & Figures for Hispanics / Latinos 2015–2017. Atlanta:American Cancer Society [Google Scholar]
- 40.Meneses K, Gisiger-Camata S, Schoenberger YM, et al. (2015) Adapting an evidence-based survivorship intervention for Latina breast cancer survivors. Women’s Heal 11:109–119. doi: 10.2217/whe.14.65 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 41.Greenlee H, Gaffney AO, Aycinena AC, et al. (2016) Long-term diet and biomarker changes after a short-term intervention among Hispanic breast cancer survivors: The !Cocinar Para Su Salud! Randomized controlled trial. Cancer Epidemiol Biomarkers Prev 25:1491–1502. doi: 10.1158/1055-9965.EPI-15-1334 [DOI] [PMC free article] [PubMed] [Google Scholar]

