Clinical Nutrition xxx (2015) 1e7
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Original article
Effect of specific educational program on dietary change and weight loss in breast-cancer survivors Concetta Finocchiaro*, Marta Ossola, Taira Monge, Maurizio Fadda, Laura Brossa, Vilma Caudera, Antonella De Francesco della Salute e della Scienza, Turin, Italy Department of Clinical Nutrition, Hospital Citta
a r t i c l e i n f o
s u m m a r y
Article history: Received 18 November 2014 Accepted 26 May 2015
Aims: Consumption of Western foods with high dietary glycemic load is associated with breast cancer development, whereas adherence to Mediterranean diet has been linked to a reduced risk. Changing lifestyle can decrease risk of recurrences and mortality. Thus decreasing the weight, improving the diet and promoting lifestyle are among of the most important issues of public health. We evaluated the effects of a specific educational intervention conducted by dietitians, nutritionists physicians, oncologist and sport physician to promote lifestyle in breast cancer survivors. Methods: We recruited 100 pts in breast cancer follow up. The intervention program consisted of four meetings once a week including lectures, training sessions and workshops lasting overall a month. Dietary recommendations were provided on the basis of WCRF/AICR guidelines and were modelled on Mediterranean diet. Sport physician recommended adapted physical activity, based on clinical experiences and scientific evidences. Results: Significantly decrease of BMI and waist circumference was observed after 2 and 6 months. Adherence to Mediterranean diet was significantly improved, both in heightening typical Mediterranean foods, both in decreasing consumption of non typical foods. At baseline 63% of women was inactive, 37% was mild active and 0% active, while at the end inactive patients felt by half (30%) and mild active women almost doubled (67%). Conclusions: We found this dietary intervention effective in reducing BMI and waist circumference, and enhancing healthy lifestyle in BC survivors. It has surely contributed to achieve these results besides the change in diet quality, mostly a marked reduction in sedentary habits. © 2015 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. All rights reserved.
Keywords: Breast cancer Weight loss Mediterranean diet
1. Introduction Breast cancer (BC) is the most common female cancer in Western Europe and North America; the risk of recurrences following treatment for early-stage disease is remarkable and it is influenced by many patient and tumor characteristics [1]. Increased incidence and mortality for breast cancer are associated with obesity. It negatively impacts disease-free survival, local recurrences and death if it is ascertained at diagnosis both during and after treatment [2e8]. Changing lifestyle can result in reduced risk of breast cancer recurrences and associated mortality [9e11].
* Corresponding author. Tel.: þ39 3282352211; fax: þ39 0116334397. E-mail address: cfi
[email protected] (C. Finocchiaro).
Metabolic alterations such as elevated insulin and glucose serum level, insulin resistance and metabolic syndrome has been associated with also BC recurrences and worse outcomes for multifactorial reasons [12e15]. Besides obesity in cancer survivors seems to increase risk of chronic diseases such as heart failure, coronary artery disease, hypothyroidism, osteoporosis and second primary malignancies [16,17]. Thus decreasing the weight, improving the diet and promoting active lifestyle are among of the most important issues of public health actually [18,19]. Important scientific societies and researchers have stated the need to implement tools and policies required to reduce the impact of obesity on cancer risk and outcomes [3,20,33]. A number of dietary intervention trials have been conducted in breast cancer survivors to improve health outcomes and to promote changes in body weight [21e30].
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It prompts the question about which approaches are more effective, given the reduced adherence to healthy eating habits over time and the lack of physical activity in cancer survivors [20,31e33]. In this study we evaluated the effects of a specific educational interventions based on group meetings and individualized followup aimed to promote health in breast cancer survivors. It was based on Mediterranean diet pattern and it included promotion of physical exercise. 2. Subjects and methods Data were derived from a dietary intervention study conducted in a sample of 100 women previously treated for non advanced breast cancer. Patients were recruited in a single centre, the della Salute of Department of Clinical Nutrition of Hospital Citta Turin from September 2009 to March 2010 by physicians, surgeons and nurses involved in breast cancer follow up. Women have participated in the program on a voluntary basis; all of them completed the study. Exclusion criteria were: vital organ involvement (renal and/or heart failure, cirrhosis) and metastases, disease and age >70 y. This study received ethic clearance by the Department of Medical Sciences and by the Breast Unit of the oncology network. 2.1. Patient characteristics Age, anthropometrics data, sedentary habits before intervention, tumour and chemotherapy characteristics are summarized in Table 1. In Table 2 are summarized the blood test at the baseline. Mean age at inclusion was 55.5 years (SD 9.3). Approximately one third was overweight (35%) and about one third was obese (35%). Mean BMI at inclusion was 28.7 and mean body weight differs significantly with weight before disease (71.8 kg vs 67.4, p < 0.001). Mean waist circumference at inclusion was above the cut-off used in diagnostic criteria for metabolic syndrome (95.3 cm, SD 13.1). Majority of patients was sedentary with insignificant time spent in physical activity (mean hour nil, SD 0.8) at baseline. The patients had already been subjected to surgical treatment in the previous year and they had completed any chemotherapy treatments from 6 months, 76% received hormonal therapy at the baseline. 2.1.1. Intervention program The intervention program consisted of four meetings once a week of two hours including lectures, training sessions and workshops lasting overall a month (Table 3). The recruitment of patients and the organization of the course was done by a nurse leader who is in charge of all the practical management of the course. It was not mandatory, but it was offered to all patients referred to the Breast Unit; those who could not attend they couldn't come for transport or labor problems. The groups were composed of about 30 people and team members did not change during the entire duration of the course. In the first lesson the team leader explained the goal of the intervention and planning meetings. The oncologist illustrated the
Table 1 The overall content of the educational intervention. Lesson
Topic
1 2 3 4
Identifying goals of course, overview lifestyle and cancer Overview nutritional values, how to reduce energy density of diet Physical activity, scientific update about exercise Refine meal plan, portion control, interruptions and holidays
Table 2 Blood test at baseline of study population. All values are expressed as mean ± SD. n. 100
Mean ± SD at the baseline
Serum glucose Total cholesterol LDL-c HDL-c Triglycerides
5.28 5.4 3.3 0.5 1.1
± ± ± ± ±
0.05 0.1 0.1 0.05 0.06
Abbreviations: LDL-low-density lipoprotein cholesterol, HDL-c high-density cholesterol.
scientific rationale of the correlation between diet and cancer and explained the evidence on the importance of a healthy lifestyle for cancer survivors. In the second lesson the nutritionist and dietitian explained that the main goal of the dietary advices is to promote reduction in energy intake. They provided information about the dietary changes, the correct choice of food pairings, portion control, the caloric density of the food and how to manage the feeling of hunger. They illustrated how to understand nutritional labels, select seasonal and traditional foods, increase use and variety of typical Mediterranean foods, and avoid or reduce non-Mediterranean foods (soft drinks, red meats, refined carbohydrates). Dietary recommendations were provided on the basis of WCRF/AICR guidelines and were modelled on Mediterranean diet. Information about food composition and contents in microelements were also given, focusing especially on antioxidants. The third lesson is entirely conducted by the sports physician who talked about the benefits of physical activity, the timing and type of physical exercise that should be done and how to maintain it over time. Sport physician illustrated also harmful consequences of a sedentary lifestyle, based on clinical experiences and scientific evidences. In summary, our team has recommended at least 3 h per week of brisk physical activity, stressing two essential criteria: gradualness and constancy. The last lesson was devoted to changes in the food strategies within the family, breaks and resumption of diet and how to behave during the lunches and social occasions.
Table 3 Characteristics of study population. All values are expressed as mean ± SD. n. 100
Mean ± SD at the baseline
Age years Stage (%) 0 (TisN0) I (T1N0) II (T1N1, T2N*, T3N0) III (T3N*) Chemotherapy regimes (%) No chemotherapy AC or EC CMF FEC Radiation therapy % Yes/No Body Weight Kg Weight before disease kg BMI BMI 25e29.9, n, % BMI 30e40, n, % BMI >40, n, % BMI before disease Waist circumference cm Endocrine therapy n %
55.5 ± 9.3
Phisical activity/hours per week
15 32 40 13 66 18 6 20 99.4/0.6% 71.8 ± 15 67.4 ± 12.4 p < 0.001 28.7 ± 5.9 35-35% 30-30% 5-5% 26.5 ± 4.8 95.3 ± 13.1 YES 76% NO 24% 0.4 ± 0.8
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At the end of the course is given an appointment for control visit. After two (T1) and six months (T2) from training course, two individual medical checks were conducted to evaluate adherence to recommendations on diet and physical activity and to assess anthropometrics measures and tailored physical activity was prescribed. The counselling intervention was based on cognitivebehavioural strategies, included self-improvement, reinforcement, practical advices, dysfunctional behaviours prevention, encouraging self-monitoring and motivation by others members of the group. The team was specifically trained to promoting healthy lifestyles and physical activity.
activity for each participant. We classified into three categories: inactive: 0; mildly active >0e9 MET-hours/week; active >9 METhours/week.
2.1.2. Goals The goals of the program were: weight loss and reduction in waist circumference if patients were overweight or obese (BMI > 24.9 and/or waist circumference > 88 cm) and increase of physical activity assessed by IPAQ questionnaire; the increase of adherence to Mediterranean diet measured by Italian Mediterranean Index.
2.2.2. Statistical analyses The data are presented as mean ± SD. Categorical variables were compared using the c2-test or Fisher test when appropriated, the continuous variable using unpaired Student's t-test. Alternatively, ANOVA was used for comparison of continuous variable between three or more groups. Logistic regression was used to evaluate the relationship between predictive factors for weight and waist circumference loss (no/yes ¼ 0/1) as dependents variables and possible predictors as the independent variables. The model was estimated using the stepwise backward method. In this multivariate analysis we used the variable that resulted in statistically significant difference in unvaried examination using a non parametric analysis like ManneWhitney U test or KruskaleWallis test. A two-tailed P-value of 0.05 or less was considered significant. All analyses were performed using StatsDirect Statistical Software version 3.0.86.
2.1.3. Dietary questionnaires and score of diet quality Food Frequency Questionnaire was used to assess dietary habits and food intake patterns [34]. The dieticians instructed women how to record food intake and estimated food servings using the photographic atlas [35]. To evaluate the quality of diet after two months we decided to use Italian Mediterranean Index, developed by Italian researchers by adapting the Greek Mediterranean Index to Italian eating behaviour [36,37]. It is based on a priori defined pattern and measures adherence to a Mediterranean diet: it is calculated from intake of 11 items comprehending typical Mediterranean foods (pasta, typical Mediterranean vegetables, fruits, legumes, olive oil and fish) and non typical Mediterranean foods (soft drinks, butter, red meat, and potatoes). If consumption of typical Mediterranean foods was in the 3rd tertile of the distribution, the person received 1 point; all other intakes received 0 points. If consumption of nonMediterranean foods was in the 3rd tertile of the distribution, the person received 1 point. Possible scores ranged form 0 to 11. 2.2. Physical activity To assess physical activity, including recreational, occupational, and household activities we used the interview-administered IPAQ questionnaire [38]. Participants reported the type, duration and frequency of physical activities and then we classified each activity according to its corresponding metabolic equivalent of task (MET) value. For all activities with MET values > 3, we summed the products of activity MET values and hours spent in each activity to arrive at MET-hours/week spent in moderate/vigorouseintensity
2.2.1. Anthropometric measures Height, weight and waist circumference were given at the first session and after two and six months from the beginning of the study. Height and weight were measured to the nearest 0.1 cm and 0.1 kg respectively, using a balance rocker fitted with stadiometer. Patients were weighed without shoes and with light clothing. Waist circumference was measured to the nearest 0.1 cm with tape measure.
3. Results 3.1. Changes in anthropometrics data Significant decrease of BMI and waist circumference was observed after two months (T1) and six months (T2), as shown in Table 4. Mean rate of weight loss was 4.2% at the end of follow up and 43% of patients had lost >5% of initial weight. Mean rate of waist circumference loss >10% was reached in 19% of women at the end of follow up. Patients were divided according to the type of BMI between 25 and 29.9, between 30 and 34.9, and 35e39.9, to see if they could be differences depending on the BMI of the beginning (Table 5). 3.2. Physical activity Other goal of the study was reducing sedentary habits of the patients. Physical activity including recreational, occupational, and household activities assessed with IPAQ questionnaire was significantly increased at the end of follow up, with 1071 METS/hours/
Table 4 Anthropometrics data after intervention at baseline (T0), after two months (T1) and six months (T2). All values are expressed as mean ± SD. n. 100
T0
T1
T2
p
Weight, Kg Weight loss, kg Weight loss, % Weight loss >5%, n BMI Waist circumference, cm Waist circumference loss, cm Waist circumference loss from >5% to 10% Waist circumference loss >10%
73 ± 15
70.8 ± 13.8 2.2 ± 3.2 2.8 ± 3.6 16% 27.9 ± 5.5 91.4 ± 14.4 3.9 ± 4.0 25% 8%
69.7 ± 13.3 3.4 ± 3.8 (vs T0) 4.2 ± 4.3 43% 26.7 ± 5.4 90 ± 11.9 5.3 ± 5.1 (vs T0) 34% 19%
<.001 <.001 <.001 <.001 <.001 <.001 <.001 ns ¼.043
28.7 ± 5.9 95.3 ± 13.1
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Table 5 Anthropometrics data after intervention at baseline (T0), after two months (T1) and six months (T2) categorized by BMI. All values are expressed as mean ± SD.
BMI 25e29.9 (n. 34) Weight, Kg Weight loss, kg Weight loss, % Weight loss >5%, n BMI Waist circumference, cm Waist circumference loss, cm Waist circumference loss from >5% Waist circumference loss >10% BMI 30e34.9 (n. 20) Weight, Kg Weight loss, kg Weight loss, % Weight loss >5%, n BMI Waist circumference, cm Waist circumference loss, cm Waist circumference loss from >5% Waist circumference loss >10% BMI 35e39.9 (n 10) Weight, Kg Weight loss, kg Weight loss, % Weight loss >5%, n BMI Waist circumference, cm Waist circumference loss, cm Waist circumference loss from >5% Waist circumference loss >10% BMI >40 (n. 5) Weight, Kg Weight loss, kg Weight loss, % Weight loss >5%, n BMI Waist circumference, cm Waist circumference loss, cm Waist circumference loss from >5% Waist circumference loss >10%
T0
T1
T2
p
70.8 ± 5.9
38.9 ± 5.8 2 ± 2.3 2.8 ± 3.6 23% 27 ± 1.8 89.4 ± 5.9 5.1 ± 4.1 29% 17%
67.4 ± 5.8 3.4 ± 2.8 (vs T0) 4.2 ± 4.3 44% 26.5 ± 1.9 87.8 ± 5.9 6.6 ± 4.9 (vs T0) 41% 26%
<.001 <.001 <.001
78.3 ± 6.1 2.8 ± 2.9 3.4 ± 2.1 10% 31.4 ± 1.4 99.8 ± 6.8 4.2 ± 4.0 30% 5%
77 ± 6.3 4.1 ± 2.0 (vs T0) 5 ± 2.3 55% 30.9 ± 1.6 96.9 ± 5.6 7.1 ± 5.4 (vs T0) 35% 20%
<.001 <.001 <.001
88 ± 8.3 5.3 ± 7.7 5.5 ± 7.9 20% 41.1 ± 1.3 108.7 ± 6.0 4.4 ± 5.3 10% 0%
86 ± 7.7 7.3 ± 8.1 (vs T0) 7.5 ± 8.2 60% 40.4 ± 1.0 107.3 ± 4.4 5.8 ± 5.0 (vs T0) 50% 10%
¼.02 <.001 <.001
102.3 ± 12 3.9 ± 2.2 3.5 ± 1.6 16% 27.9 ± 5.5 112.6 ± 5.3 3.4 ± 3.2 40% 0%
100.6 ± 10.9 5.6 ± 3.4 (vs T0) 5.1 ± 2.6 43% 26.7 ± 5.4 109.6 ± 6.0 6.4 ± 3.5 (vs T0) 60% 0%
¼.01 ¼.01 ¼.04
27.8 ± 1.5 94.4 ± 5.3 to 10%
81.1 ± 6.5
32.6 ± 1.4 104 ± 6.2 to 10%
93.3 ± 7.7
36.9 ± 1.0 113 ± 6.1 to 10%
106 ± 13.9
42.6 ± 2.0 116 ± 7.6 to 10%
week vs 507 METS/hours/week respectively (p < 0.001). At baseline 63% of women was inactive, 37% was mild active and 0% active while at the end of follow up inactive patients felt by half (30%) and mild active women almost doubled (67%) according to intensity of physical activity measured in MET-hours/week. Results are summarized in Table 6.
<.001 <.001 <.001
<.001 <.001 <.001
<.001 ¼.02 <.001
¼.004 ¼.02 ¼.05
p < 0.001, 38 g/die vs 24 g/die, p < 0001 and 64 g/die vs 39 g/die, p ¼ 0.001. All component of non typical Mediterranean foods were significantly reduced in eating habits of the sample; results are reported in two different table, one for aliments with daily consumption (Table 8), one table for aliments whose consumption frequency is per week (Table 9).
3.3. Adherence to Mediterranean diet Adherence to Mediterranean diet was significantly improved, both in heightening typical Mediterranean foods, both in decreasing consumption of non typical Mediterranean foods, as shown by the results reported in (Table 7.) In particular, it must be noted increased frequency of vegetables, pulses and fish consumption, respectively 388 g/die vs 224 g/die,
Table 6 Physical activity, METS/hours/week at a T0 and T2. All values are expressed as mean ± SD. n. 100
T0
Physical activity, METS/hours/week 8.4 ± 7.3 Intensity of physical activity 63% inactive MET/hours/week 37% mild active 0% active
T2
p
17.8 ± 12.4 30% inactive 67% mild active 3% active
<.0001 <.0001 <.0001 ns
3.4. Predictive factors for weight and waist circumference loss on multivariate analysis. On logistic regression model all the item of Mediterranean index and frequency of physical activity at each time of the study were
Table 7 Change in frequency of typical mediterranean foods at baseline and at T1 and T2. All values are expressed as mean ± SD. n. 100
T0
Pasta, g/day Vegetables, g/day Fruit, g/day Pulses, g/day Olive oil, g/day Fish, g/day
27.8 224.5 361 24.3 43.4 39.2
T1 ± ± ± ± ± ±
33.7 103.6 186.8 0.2 11.1 34.7
33.5 322.5 386.5 38.8 38 76.3
T2 ± ± ± ± ± ±
32 116.5 21.8 21.8 8.5 36.5
23.1 388.2 400.9 38.5 38.4 64.3
p(vs T0) ± ± ± ± ± ±
25.4 130.1 128.8 26.3 7 37.2
¼.2 <.001 ¼.04 <.0001 ¼.0004 ¼.0001
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C. Finocchiaro et al. / Clinical Nutrition xxx (2015) 1e7 Table 8 Change in frequency of non typical mediterranean foods with daily consumption at baseline and at T1 and T2. All values are expressed as mean ± SD.
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Table 10 Predictive factors for waist circumference loss on Logistic regression model adjusted for BMI pre-disease, age, radiotherapy, chemotherapy.
n. 100
T0
T1
T2
p(vs T0)
Variable
Odds ratio
95% CI
P
Red Meat, g/day Potatoes, g/day Alcohol, g/day
35.1 ± 20.4 18.6 ± 17.4 4.5 ± 6.3
19.6 ± 17.2 10.3 ± 15.1 2.7 ± 4.8
15 ± 14.3 12.9 ± 15.5 1.9 ± 4
<.001 ¼.015 ¼.0009
Read meat at T0 Physical activity, hour at T2
0.9378 1.7523
0.8941 to 0.9836 1.0135 to 3.0299
0.008277 0.04466
tested. We adjusted for BMI before cancer, age and the treatment (chemo- and radiotherapy). Only few factors were significant to predict circumference loss (Table 10) and waist circumference loss (Table 11).
4. Discussion In this study we found that a dietary intervention is effective in reducing BMI and waist circumference, enhancing diet quality in BC survivors. Association with the increase in physical activity may account for the positive effects observed. Weight gain after BC treatment has been well studied over the last decades; the mean weight change reported in literature was 1e6 kg [39,40]. Recently a French prospective study has shown that in a cohort of French women with early breast cancer 40% had BMI 25 at the time of diagnosis and 60% gained weight after adjuvant chemotherapy [41]. It is stated that appropriate nutritional management and physical activity programs are needed in these setting. Many other study have investigated the relationship between dietary interventions and weight loss in BC survivors but few have focused on Mediterranean-like dietary pattern [21,22]. Increased assumption of various non starchy vegetables and fruits, unprocessed cereals and pulses and reduced intake of fats and sweets are the current WCRF recommendations on diet evaluated for cancer prevention. Adherence to these guidelines has been also associated with reduced mortality from cancer, circulatory and respiratory diseases [42e44]. Based on these assumptions we designed our intervention on the prescription of a dietary pattern containing high proportions of fruit, vegetables, and pulses, unprocessed cereals, a low-tomoderate intake of dairy product and a low intake of meat according with the Mediterranean diet. In this sample, although patients came from a country that was part of Mediterranean diet culture, habits at baseline was far from Mediterranean pattern. Besides 35% of patients was overweight and 35% was obese. After the educational programme eating habits were significantly changed and a meaningful adherence to dietary recommendations was reached. Remarkable results are a tripled consumption of pulses and the achievement of three fish servings per week, that is the minimum recommended amount. Regarding the intake of pasta, portions remains almost unchanged but the use of whole grains has largely increased (results not shown). The reduction in weekly intake of non typical Mediterranean foods was 25% for sugar and sweets sugar drinks and 23% for red meat.
Table 9 Change in frequency of non typical mediterranean foods with weekly consumption at baseline and at T1 and T2. All values are expressed as mean ± SD. n. 100
T0
T1
T2
p(vs T0)
Butter, g/week Soft drinks, g/week
5.4 ± 8.9 31.7 ± 74.4
2.6 ± 7.7 6.6 ± 28.2
1.5 ± 4.6 5.6 ± 24.5
¼.00014 ¼.001
To assess the suitability of quality diet obtained with nutritional follow up, we decided to use Italian Mediterranean Index. Highest score has been related to reduced risk of colon cancer and stroke in Italian population [36,37]. We resolved to employ it, because it is proceeded specifically from Italian population and it appears more suitable as well as more sensitive for capturing aspects of diet that are healthy. However greater adherence to Mediterranean diet was related to enhanced weight loss at the end of follow up, as a score of at least 8 in Mediterranean Index is resulted a significant predict factor in the logistic regression analysis. It was also shown that the patients who were eating less red meat and less butter at the beginning of the study, had lost more weight and their waist size was reduced more considerably than the other patients. The main reason of these different results could be that the first patients had better eating habits. The predict factors in the logistic regression model were still significant after adjustment for possible confounders. In particular, after adjusted for the possible effects of cancer treatment and age on outcome, quality diet and physical activity were well related to weight loss. In general, regarding weight loss and reduction in waist circumference in overweight (BMI > 24 and/or waist circumference > 88 cm) pts, we can affirm that results at the end of the study have been significant. Both median BMI and median waist circumference were closer to normal levels: 26.7 kg/cm2 vs 28 kg/ cm2 and 90 cm2 vs 95 cm respectively. Also the percentage weight loss amounted to 4.2% at six months is satisfying considering that a reduction of 10% of usual weight over one year is a commonly accepted goal of any dietetic program. The patients lost weight significantly over time studied regardless of the type of BMI to which they had been grouped. After the intervention 34% of patients was still overweight and 27% was obese. It should be pointed out in agreement with the comment of Alfano et al. that we had not assess body composition and we can suspect that the measurement of only BMI may lead to missed diagnoses of sarcopenic obesity, a condition that may adversely affect risk of chronic and late effects, and poor prognosis [33]. We can't use any methods for assessing body composition because courses and visits were held outside our ward. Weight loss intervention combined with exercise can improve body composition, increase muscle mass and reduce body fat. Although we can't affirm that body composition in our patients changed after diet and physical activity, previous studies showed the effects of a multi-level intervention on body composition detected with the gold standard method, like DEXA [26].
Table 11 Predictive factors for weight loss % on Logistic regression model adjusted for BMI pre-disease, age, radiotherapy, chemotherapy. Variable
Odds ratio
95% CI
Butter at T0 Pulses at T2 Mediterranean index ¼ 8 at T2 Physical activity, hour at T2
0.957 0.966 6.012 1.563
0.791 0.934 1.232 1.057
to to to to
P 0.964 0.989 39.120 2.230
0.037 0.046 0.039 0.038
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In our sample it was observed a marked reduction in sedentary habits. So at the end of follow up 70% of patients was no more inactive. Intensity of physical activity measured by MET-hours/ week significantly enhanced after the educational program and that could have a role in counteracting loss of muscle mass besides promoting and maintaining weight loss. In the logistic regression analysis increased physical activity (in term of increased time spent in) is resulted significantly effective in reducing weight and waist circumference according to amount of data of literature [45]. It is consistently observed in many case that physical exercise more than dietetic intervention results in weight loss in obese subjects. Finally it is well known the difficulty in keeping the change in lifestyle, so we have decided to manage the follow up with a tailored pathway for each subject. Our protocol providing regular visits directly with the patient and not by mail or telephone recall. It has allowed us to create and maintain a personal relationship with the patient by interacting with the individual psychological aspects and then determining probably better adherence to the dietetic program. In our experience an approach ad personam may have an important value because it allows a more incisive and direct relationship with patients and acts on personal or family dynamics that can be an obstacle for the continuation of the result. This study has some limitations: the duration of follow up are limited so that we cannot know if the results can be generalized and if the intervention might have lasting effects. About estimation of physical activity we think that it should find even more specific assessment tools in order to study it in detail. In conclusion, the results are encouraging but larger and longer clinical trials are needed to investigate the lasting effects of intervention and their relation with prognosis. Statement of authorship CF conceived of the study, was involved in patient management and drafted the manuscript. MO was involved in the interpretation of data and drafted the manuscript. TM was involved in patient dietary management and collection and interpretation of data. LB was involved in patient dietary management. MF carried out statistical analysis. VC was involved in patient dietary management. ADF provided general support. Conflict of interest No conflict of interest declared. Transparency document
[7]
[8]
[9]
[10] [11] [12]
[13]
[14]
[15]
[16]
[17]
[18]
[19]
[20]
[21]
[22]
[23]
[24]
[25]
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Transparency document related to this article can be found online at http://dx.doi.org/10.1016/j.clnu.2015.05.018. [27]
References [1] American Cancer Society, Cancer facts and Figures. Atlanta: American Cancer Society; 2014. p. 2014. [2] Azrad M, Demark-Wahnefried W. The association between adiposity and breast cancer recurrence and survival: a review of the recent literature. Curr Nutr Rep 2014;3:9e15. [3] Ligibel JA, Alfano CM, Courneya KS, Demark-Wahnefried W, Burger RA, Chlebowski RT, et al. American society of clinical oncology position statement on obesity and cancer. J Clin Onc 2014;32:3568e74. [4] Kroenke CH, Chen WY, Rosner B, Holmes MD. Weight, weight gain and survival after breast cancer diagnosis. J Clin Oncol 2005;23:1370e8. [5] Kumar NB, Cantor A, Allen K, Cox CE. Android obesity at diagnosis and breast carcinoma survival. Cancer 2000;12:2751e7. [6] Irwin ML, McTiernan A, Baumgartner RN, Baumgartner KB, Bernstein L, Gilliland FD, et al. Changes in body fat and weight gain after a breast cancer
[28]
[29]
[30]
[31]
diagnosis: influence and demographic, prognostic, and lifestyle factors. J Clin Oncol 2005;23:774e82. Litton WL, Gonzales-Angulo AM, Warneke CL, Buzdar AU, Kau SW, Bondy M, et al. Relationship between obesity and patologic response to neoadjuvant among women with operable breast cancer. J Clin Oncol 2008;26:4072e7. Chan DSM, Vieira AR, Aune D, Bandera EV, Greenwood DC, McTiernan A, et al. Body mass index and survival in women with breast cancer-systematic literature review and meta-analysis of 82 follow-up studies. Ann Onc 2014;00:1e14. Rock CL, Doyle C, Demark-Wahnefried W, Meyerhardt J, Courneya KS, Schwartz AL, et al. Nutrition and physical activity guidelines for cancer survivors. CA Cancer J Clin 2012;62:242e74. WCRF. Continuous Update Project. Diet, Nutrition, Physical Activity and Breast Cancer Survivors. 2014. Chlebowski RT. Nutrition and physical activity influence on breast cancer incidence and outcome. Breast 2013;22:30e7. Rosato V, Bosetti C, Talamini R, Levi F, Montella M, Giacosa A, et al. Metabolic syndrome and the risk of breast cancer in postmenopausal women. Ann Oncol 2011 Dec;22(12):2687e92. Bhandari R, Kelley GA, Hartley TA, Rockett IR. Metabolic syndrome is associated with increased breast cancer risk: a systematic review with meta-analysis. Int J Breast Cancer 2014. 2014: 189384. Pasanisi P, Berrino F, De Petris M, Venturelli E, Mastroianni A, Panico S. Metabolic syndrome as a prognostic factor for breast cancer recurrences. Int J Canc 2006;119:236e8. Healy LA, Ryan AM, Carroll P, Ennis D, Crowley V, Boyle T, et al. Metabolic syndrome, central obesity and insulin resistance are associated with adverse pathological features in postmenopausal breast cancer. Clin Onc 2010;22: 281e8. Khan NF, Mant D, Carpenter L, Forman D, Rose PW. Long-term health outcomes in a British cohort of breast, colorectal and prostate cancer survivors: a database study. BJ Cancer 2011;105:29e37. Weaver KE, Foraker RE, Alfano CM, Rowland JH, Arora NK, Bellizzi KM, et al. Cardiovascular risk factors among long-term survivors of breast, prostate, colorectal, and gynaecologic cancers: a gap in survivorship care? J Cancer Surviv 2013;7:253e61. Eheman C, Henley SJ, Ballard-Barbash R, Jacobs EJ, Schymura MJ, Noone AM, et al. Annual report to the nation on the status of cancer, 1975e2008, featuring cancers associated to excess weight and lack of sufficient physical activity. Cancer 2012;118:2338e66. Eccles SA, Aboagye EO, Ali S, Anderson AS, Armes J, Berditchevski F, et al. Critical research gaps and translational priorities for the successful prevention and treatment of breast cancer. Breast Cancer Res 2013;15:3e11. Demark-Wahnefried W, Aziz NM, Rowland JH, Pinto BM. Riding the crest of the teachable moment: promoting long-term health after the diagnosis of cancer. J Clin Oncol 2005;23:5814e30. Pierce JP, Natarajan L, Caan BJ, Parker BA, Greenberg ER, Flatt SW, et al. 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 2007 Jul 18;298(3):289e98. Villarini A, Pasanisi P, Raimondi M, Gargano G, Bruno E, Morelli D, et al. Preventing weight gain during adjuvant chemotherapy for breast cancer: a dietary intervention study. Breast Cancer Res Treat 2012 Sep;135(2):581e9. Pakiz B, Flat SV, Bardwel WA, Rock CL, Mills PJ. Effects of a weight loss intervention on body mass, fitness and inflammatory biomarkers in overweight or obese breast cancer survivors. Int J Behav Med 2011;18:333e41. Christy SM, Mosher CE, Sloane R, Snyder DC, Lobach Df, DemarkWahnefried W. Long-term dietary outcomes of FRESH START intervention for breast and prostate Cancer survivors. J Am Diet Assoc 2011;111:1844e51. Scott E, Daley AJ, Doll H, Woodroofe N, Coleman RE, Mutrie N, et al. Effects of an exercise and hypocaloric healthy eating program on biomarkers associated with long-term prognosis after early-stage breast cancer: a randomized controlled trial. Cancer Causes Control 2013 Jan;24(1):181e91. Demark-Wahnefried W, Case LD, Blackwell K, Marcom PK, Kraus W, Aziz N, et al. Results of a diet/exercise feasibility trial to prevent adverse body composition change in breast cancer patients on adjuvant chemotherapy. Clin Breast Cancer 2008;8(1):70e9. Demark-Wahnefried W, Morey MC, Sloane R, Snyder DC, Miller PE, Hartman TJ, et al. Reach out to enhance wellness home-based diet-exercise intervention promotes reproducible and sustainable long-term improvements in health behaviors, body weight, and physical functioning in older, overweight/obese cancer survivors. J Clin Oncol 2012;30:2354e61. Rock CL, Byers TE, Colditz GA, Demark-Wahnefried W, Ganz PA, Wolin KY, et al. Reducing breast cancer recurrences with weight loss, a vanguard trial: the Exercise and Nutrition to Enhance Recovery and Good Health for You (ENERGY) Trial. Contemp Clin Trials 2013:282e95. Goodwin PJ, Segal RJ, Vallis M, Ligibel JA, Pond JR, Robidoux A, et al. Randomized trial of a telephone-based weight-loss intervention in postmenopausal women with breast cancer receiving letrozole: the LISA trial. J Clin Oncol 2014;32:2231e9. Reeves MM, Terranova CO, Eakin EG, Demark-Wahnefried W. Weight loss intervention trials in women with breast cancers: a systematic review. Obes Rev 2014;15:749e68. Milliron BJ, Vitolins MZ, Tooze JA. Usually dietary intake among female breast cancer survivors is not significantly different from women with no cancer
Please cite this article in press as: Finocchiaro C, et al., Effect of specific educational program on dietary change and weight loss in breast-cancer survivors, Clinical Nutrition (2015), http://dx.doi.org/10.1016/j.clnu.2015.05.018
C. Finocchiaro et al. / Clinical Nutrition xxx (2015) 1e7
[32]
[33]
[34]
[35] [36]
[37]
[38]
history: results of the National Health and Nutrition Examination Survey, 2003e2006. J Acad Nutr Diet 2014;114:932e7. Bourke L, Homer KE, Thaha MA, Steed L, Rosario DJ, Robb KA, et al. Interventions for promoting habitual exercise in people living with and beyond cancer. Cochrane Database Syst Rev 2013;(9). http://dx.doi.org/10.1002/ 14651858.CD010192.pub2. Art. No.: CD010192. Alfano CM, Molfino A, Muscaritoli M. Interventions to promote energy balance and cancer survivorship: European and North American priorities for research and care. Cancer 2013;119:2143e50. Franceschi S, Negri E, Salvini S, Decarli A, Ferraroni M, Filiberti R, et al. Reproducibility of an Italian food frequency questionnaire for cancer studies: results for specific food items. Eur J Cancer 1993;29A(16):2298e305. Fantuzzi A, Chiuchiu M, Bedogni G. Atlante fotografico “Scotti Bassani” delle porzioni degli alimenti. Istituto Scotti Bassani; 2005. p. 1e104. Agnoli C, Krogh V, Grioni S, Sieri S, Palli D, Masala G, et al. A priori-defined dietary patterns are associated with reduced risk of stroke in a large Italian cohort. J Nutr 2011;141:1552e8. Agnoli C, Grioni S, Sieri S, Palli D, Masala G, Sacerdote C, et al. Italian Mediterranean index and risk of colorectal cancer in the Italian section of the EPIC cohort. Int J Cancer 2012;132:1404e11. Craig CL, Marshall AL, Sjostrom M, Bauman AE, Booth ML, Ainsworth BE, et al. International physical activity questionnaire: 12-country reliability and validity. Med Sci Sports Exerc 2003 Aug;35(8):1381e95.
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[39] Saquib N, Flatt SW, Natarajan L, Thomson CA, Bardwell WA. Weight gain and recovery of pre-cancer weight after breast cancer treatment: evidence from the women's healthy eating and living (WHEL) Study. Breast Cancer Res Treat 2007;105:177e86. [40] Goodwin PJ, Ennis M, Pritchard KL. Adjuvant treatment and onset of menopause predict weight gain after cancer diagnosis. J Clin Oncol 1999;17:120e9. [41] Tredan O, Bajard A, Meunier A, Roux P, Fiorletta I, Gargi T, et al. Body weight change in women receiving adjuvant chemotherapy for breast cancer: a French prospective study. Clin Nutr 2010;29:187e91. [42] Vergnaud AC, Romaguera D, Peeters PH, van Gils CH, Chan DS, Romieu I, et al. Adherence to the World Cancer Research Fund/American Institute for Cancer Research guidelines and risk of death in Europe: results from the European Prospective Investigation into Nutrition and Cancer cohort study. Am J Clin Nutr 2013;97:1107e20. [43] Sofi F, Abbate R, Gensini GF, Casini A. Accruing evidence on benefits of adherence to the Mediterranean diet on health: an update systematic review and meta-analysis. Am J Clin Nutr 2010;92:1189e96. [44] Trichopoulou A, Costacou T, Bamia C, Trichopoulos D. Adherence to a Mediterranean diet and survival in a Greek population. NEJM 2003;348:2599e608. [45] Conn VS, Hafdahl A, Phillips LJ, Ruppar TM, Chase JA. Impact of physical activity interventions on anthropometric outcomes: systematic review and meta-analysis. J Prim Prev 2014;35:203e15.
Please cite this article in press as: Finocchiaro C, et al., Effect of specific educational program on dietary change and weight loss in breast-cancer survivors, Clinical Nutrition (2015), http://dx.doi.org/10.1016/j.clnu.2015.05.018