Abstract
Purpose
Physical activity is associated with reduced risk and progression of breast cancer, and exercise can improve physical function, quality of life and fatigue in cancer survivors. Evidence on factors associated with cancer survivors’ adherence to physical activity guidelines from the American Cancer Society and the U.S. Department of Health and Human Services is mixed. This study seeks to help fill this gap in knowledge by examining correlates with physical activity among breast cancer survivors.
Methods
Overweight or obese breast cancer survivors (N=692) were examined at enrollment into a weight loss intervention study. Questionnaires and medical record review ascertained data on education, race, ethnicity, menopausal status, physical activity, and medical history. Measures of anthropometrics and fitness level were conducted. Regression analysis examined associations between physical activity and demographic, clinical, and lifestyle factors.
Results
Overall, 23% of women met current guidelines. Multivariate analysis revealed that body mass index (p=0.03), emergency room visits in the past year (p=0.04), and number of co-morbidities (p=0.02) were associated with less physical activity. Geographic region also was associated with level of physical activity (p=0.02), with women in Alabama reporting significantly less activity than those in other participating regions.
Conclusions
The majority of overweight/obese breast cancer survivors did not meet physical activity recommendations. Physical activity levels were associated with degree of adiposity, geographic location, and number of co-morbidities. The majority of overweight breast cancer survivors should be encouraged to increase their level of physical activity. Individualizing exercise prescriptions according to medical co-morbidities may improve adherence.
Keywords: Physical activity, breast cancer, guidelines, obesity, survivors, exercise
Introduction
Cancer is a major public health problem and is the leading cause of death among men and women in the U.S. aged 85 years and younger [1]. Between 1990/1991 and 2007, cancer death rates decreased by 22.2% in men and by 13.9% in women; however, 1 in 4 deaths in the U.S. is currently due to cancer [2]. Due to advances in early detection and treatment, 65% of Americans diagnosed with cancer now live more than 5 years. Breast cancer survivors are the largest group of cancer survivors, followed by prostate cancer survivors and colorectal cancer survivors.
Obesity is an important risk factor for postmenopausal breast cancer incidence and is a major risk factor for breast cancer recurrence and morbidity in both pre- and postmenopausal women [3–6]. Independently, physical activity is also a significant factor related to the risk and recurrence of breast cancer [7]. The Nurses’ Health Study found that in nearly 3,000 breast cancer survivors, higher levels of post-treatment physical activity were associated with a 26% to 40% reduction in risk of breast cancer recurrence, breast cancer-specific mortality, and all-cause mortality [8].
Guidelines for physical activity as they relate to various disease states have been published by the U.S. Department of Health and Human Services (US DHHS) [9]. Overall, weekly aerobic activity duration of 150 minutes of moderate-intensity exercise or 75 minutes of vigorous-intensity exercise, or some combination thereof, is currently recommended. These guidelines are endorsed by the American Cancer Society [10]. Further, the American College of Sports Medicine (ACSM) Roundtable on Exercise Guidelines for Cancer Survivors concluded that exercise training is safe during and after cancer treatment and results in improvements in physical function, quality of life and cancer-related fatigue in several cancer survivor groups [11].
Although it is recognized that any amount of physical activity is beneficial to cancer survivors, the evidence describing how much breast cancer survivors exercise and the factors associated with how well they meet the physical activity guidelines is mixed. Potential determinants of physical activity that have been examined include demographic characteristics, cancer-related variables (e.g., stage, type of treatment), degree of obesity, health status, level of aerobic fitness, and various psychosocial factors [12–17]. Level of physical activity, as well as the factors associated with physical activity, have been observed to change over time following diagnosis, as shown in a longitudinal investigation of a sample of breast cancer survivors who were followed for five years post-diagnosis [15].
This study seeks to contribute to knowledge of determinants of physical activity among breast cancer survivors by describing various characteristics associated with physical activity in a large and relatively heterogeneous sample of survivors. The results of this analysis set the stage for the longitudinal evaluation of outcomes of a behavioral intervention to promote weight loss and increase physical activity in this sample. More knowledge of influencing factors may help health care providers to develop interventions and educational programs and to prescribe exercise based on specific patient characteristics.
Methods
Design and study population
A total of 692 overweight or obese breast cancer survivors were enrolled into a randomized controlled trial of a weight loss intervention, the Exercise to Enhance Recovery and Good Health for You (ENERGY) trial, at four U.S. sites (San Diego, CA, USA; Denver, CO; St. Louis, MO; and Birmingham, AL). Inclusion criteria were: age ≥21 years; a history of breast cancer (stages I [≥1 cm], II, or III) diagnosed within the previous five years; completion of initial therapies not including endocrine therapy; body mass index (BMI) 25–45 kg/m2; and ability to comply with study procedures. Exclusion criteria included: history of malignancies other than initial breast cancer with the exception of non-melanoma skin cancer, serious psychiatric illness, and any medical condition substantially limiting moderate physical activity, such as severe orthopedic conditions. The study was reviewed and approved by the Institutional Review Boards of all sites. Informed consent was obtained from all individual participants included in the study. A detailed description of the study procedures and intervention has been published previously [18].
Measures
At the baseline visit of the ENERGY trial, questionnaires were used to collect self-reported information about education, race, ethnicity, smoking status, menopausal status, and medical history. Staff reviewed all questionnaires for completeness. Medical record review was conducted by trained staff to obtain information on breast cancer diagnosis, treatment including surgery and chemotherapy, and endocrine-modulating therapy, including aromatase inhibitors and selective estrogen-receptor modulators. Before enrollment in the study, all subjects had completed any chemotherapy and/or radiation therapy prescribed by their oncologists, and had not experienced a cancer recurrence or new cancer event.
Measures of height and weight were obtained by trained staff at the baseline clinic visit and used to calculate BMI. Physical activity was measured using the modified Godin Leisure-Time Exercise Questionnaire (GLTEQ) which has been validated previously in cancer research [19]. The modified GLTEQ consists of three questions regarding the frequency and duration of mild, moderate, and strenuous exercise performed during free time in a typical week.
Fitness level was obtained by measuring recovery heart rate after a 3-minute step test in which participants ascended and descended an 8” step for 3 minutes, using a metronome rate of 96 beats per minute. Immediately after the step test, the heart rate was measured for 30 seconds and compared to previously published standards to determine fitness level [20]. “Good to excellent” fitness corresponds to the top tertile (lowest recovery heart rate) among age-matched women in a large community health study [20] and “poor to fair” fitness corresponds to the two lower tertiles (higher recovery heart rates).
The number of co-morbidities was the sum of each of the following conditions for which the participants reported receiving treatment: heart disease, hypertension, lung disease, diabetes, ulcers or stomach disease, kidney disease, liver disease, anemia or other blood disease, depression, osteoarthritis, back pain, rheumatoid arthritis, and other conditions.
Statistical analysis
The mean (standard deviation [SD]) of minutes of reported weekly moderate-to-vigorous physical activity are presented by strata of demographic, geographic, and medical covariates. Regression analysis computed statistical significance for amount of physical activity by continuous or categorical predictors. Women reporting 150 minutes or more of weekly moderate/vigorous physical activity were categorized as “meeting guidelines” [11]. The association between meeting or not meeting physical activity guidelines and demographic, clinical and lifestyle factors was evaluated using chi-square tests (categorical variables) and ANOVA (continuous variables). A multivariate linear model examined the relationship between physical activity level (continuous) with demographic, clinical, and lifestyle variables found to be significant in the bivariate analyses at p<0.20, and contrasts between minutes per week of moderate/vigorous physical activity were compared across categories of variables. The alpha for the multivariate model was set at p<0.05. All analyses were conducted using SAS version 9.3 (SAS Institute, Inc., Cary NC).
Results
Associations between demographic and clinical characteristics and physical activity are presented in Table 1. Among the 692 study participants, the mean (SD) age at enrollment was 56 (9) years and years of education was 16 (2). The majority of the participants identified as non-Hispanic white (79%, N=547), college graduates (59%, N=410), married or with a partner (67%, N=463), and postmenopausal (87%, N=605). The majority of participants had received chemotherapy and/or radiation therapy treatments (92%, N=638) and did not experience any overnight hospitalization (75%, N=518) or emergency room visit (85%, N=586) within the year before entering the study. The majority of participants had been diagnosed with stage II breast cancer (52%, N=358) within 3 years (58%, N=401) before entering the study. Median time since diagnosis was 31 months.
Table 1.
Physical activity by demographic and cancer characteristics
| N | Minutes of moderate/vigorous physical activity mean (SD) |
p value | |
|---|---|---|---|
| Age, years | 0.81 | ||
| <50 | 173 | 102 (137) | |
| 50–64 | 372 | 92 (129) | |
| ≥65 | 147 | 101 (136) | |
| Education | 0.30 | ||
| Not a college graduate | 282 | 89 (136) | |
| College graduate | 410 | 102 (130) | |
| Race/ethnicity | 0.22 | ||
| White non-Hispanic | 547 | 93 (122) | |
| African-American | 71 | 128 (189) | |
| Hispanic | 46 | 81 (105) | |
| Asian | 11 | 122 (90) | |
| Mixed/other | 15 | 114 (233) | |
| Menopause status at study entry | 0.16 | ||
| Premenopausal/ peri-menopausal | 87 | 115 (155) | |
| Postmenopausal | 605 | 94 (129) | |
| Years between diagnosis and study entry | 0.61 | ||
| <1 | 76 | 102 (167) | |
| 1–2.9 | 325 | 93 (121) | |
| ≥3 | 291 | 100 (134) | |
| Breast cancer stage | 0.09 | ||
| I | 210 | 113 (134) | |
| II | 358 | 92 (138) | |
| III | 124 | 83 (109) | |
| Cancer treatment | 0.32 | ||
| Radiation only | 111 | 99 (137) | |
| Chemotherapy only | 136 | 97 (160) | |
| Both radiation and chemotherapy | 391 | 91 (117) | |
| Adjuvant hormone therapy | 0.31 | ||
| Aromatase Inhibitor | 366 | 98 (130) | |
| Selective estrogen receptor modulator | 147 | 108 (138) | |
| None | 179 | 85 (133) | |
| Clinical site | 0.02 | ||
| Alabama | 116 | 66 (99) | |
| California | 215 | 109 (126) | |
| Colorado | 187 | 109 (148) | |
| Missouri | 174 | 89 (139) | |
| Marital status | 0.61 | ||
| Married or partnered | 463 | 99 (131) | |
| Divorced | 99 | 75 (93) | |
| Single | 74 | 107 (170) | |
| Widowed | 41 | 101 (144) | |
| Other | 15 | 113 (139) | |
| Hospitalizations in last year | 0.17 | ||
| Any | 174 | 85 (131) | |
| None | 518 | 101 (133) | |
| Emergency room visits in the last year | 0.04 | ||
| Any | 106 | 72 (90) | |
| None | 586 | 101 (138) | |
| Number of prescription medications | <0.0001 | ||
| 0 | 135 | 133 (170) | |
| 1–2 | 292 | 100 (128) | |
| 3–4 | 181 | 79 (111) | |
| 5 or more | 84 | 67 (106) | |
| Number of co-morbidities | 0.001 | ||
| 0 | 253 | 118 (152) | |
| 1 | 240 | 93 (123) | |
| 2 | 119 | 81 (119) | |
| 3 or more | 82 | 65 (98) | |
| Smoking status | 0.60 | ||
| Current | 24 | 70 (145) | |
| Former | 219 | 96 (135) | |
| Never | 448 | 98 (130) |
Associations between medical, geographic and lifestyle characteristics and number of minutes of moderate/vigorous exercise also are shown in Table 1. As shown, there was a trend for lower levels of physical activity with higher stages of breast cancer (p=0.09). Lower levels of physical activity were reported by those who experienced an emergency room visit within a year of the study compared with those who did not (p=0.04). The number of co-morbidities was also inversely related to the amount of physical activity (p<0.0001, continuous ANOVA; p<0.001). In this bivariate analysis, there were also differences in level of physical activity across the four clinic sites (p=0.02), with survivors living in Alabama reporting far less physical activity than those living in other regions in the U.S.
The results of the bivariate analysis of physical activity within BMI and fitness level categories are shown in Table 2. As expected, the amount (minutes/week) of moderate to vigorous exercise was significantly higher among women with lower BMI (p=0.002) and higher cardiovascular fitness levels (p<0.0001).
Table 2.
Physical activity by body measurements and fitness level
| N | Minutes of moderate/vigorous physical activity mean (SD) |
P value | |
|---|---|---|---|
| Body mass index, kg/m2 | 0.002 | ||
| Overweight, 25–29.99 | 321 | 118 (145) | |
| Obese I, 30–34.99 | 219 | 80 (106) | |
| Obese II, 35–39.99 | 105 | 80 (143) | |
| Obese III, ≥40 | 47 | 68 (102) | |
| Fitness level | <0.0001 | ||
| Good to excellent | 162 | 140 (163) | |
| Poor to fair | 499 | 83 (118) |
The percentage of participants meeting the physical activity guidelines of 150 minutes/week moderate-intensity exercise across the variables of interest are shown in Table 3. Eighty-five percent of participants from Alabama did not meet the guidelines, whereas California, Colorado, and Missouri had rates of 73%, 74%, and 78%, respectively, who did not meet guidelines (p=0.07). As expected, higher BMI levels and lower fitness levels were associated with a higher percentage of participants not meeting guidelines (p=0.13 and p=0.0002, respectively). Cancer and treatment characteristics were not significantly associated with the percentage of participants meeting physical activity guidelines.
Table 3.
Percentage of participants not meeting physical activity guidelines
| Variable | % Not Meeting Guidelines |
p value |
|---|---|---|
| Age, years | 0.64 | |
| <50 | 75 | |
| 50–64 | 78 | |
| ≥65 | 74 | |
| Race/ethnicity | 0.56 | |
| White non-Hispanic | 78 | |
| African-American | 70 | |
| Hispanic | 78 | |
| Asian | 64 | |
| Mixed/other | 80 | |
| Education | 0.27 | |
| Not college graduate | 79 | |
| College graduate | 75 | |
| Body mass index, kg/m2 | 0.13 | |
| Overweight, 25–29.999 | 73 | |
| Obese I, 30–34.999 | 79 | |
| Obese II, 35–39.999 | 82 | |
| Obese III, ≥40 | 81 | |
| Fitness level | 0.0002 | |
| Good to excellent | 66 | |
| Poor to fair | 80 | |
| Menopause status at study entry | 0.33 | |
| Premenopausal/peri-menopausal | 72 | |
| Postmenopausal | 77 | |
| Years between diagnosis and study entry | 0.94 | |
| <1 | 78 | |
| 1–2.9 | 77 | |
| ≥3 | 76 | |
| Breast cancer stage | 0.25 | |
| I | 73 | |
| II | 77 | |
| III | 81 | |
| Chemotherapy | 0.26 | |
| Yes | 78 | |
| No | 73 | |
| Radiation | 0.36 | |
| Yes | 77 | |
| No | 74 | |
| Adjuvant hormone therapy | 0.36 | |
| Aromatase Inhibitor | 75 | |
| Selective estrogen receptor modulator | 75 | |
| None | 80 | |
| Clinical site | 0.07 | |
| Alabama | 85 | |
| California | 73 | |
| Colorado | 74 | |
| Missouri | 78 | |
| Smoking status | 0.73 | |
| Current | 83 | |
| Former | 76 | |
| Never | 76 | |
| Number of co-morbidities | 0.06 | |
| 0 | 72 | |
| 1 | 76 | |
| 2 | 82 | |
| 3 or more | 84 |
Results of the multivariate model of associations for minutes of physical activity, which controlled for potential influencing factors, are shown in Table 4. Beta coefficients equate to weekly minutes of moderate/vigorous physical activity compared with the reference category for categorical variables, or per unit increase for continuous measures. As in the bivariate analysis, BMI was shown to be significantly associated with the amount of physical activity reported (p=0.03). With every increase in 1 kg/m2 of BMI, there was a mean decrease of 2.5 minutes/week in physical activity. Clinical site also was found to be significant, where participants from California or Colorado showed an average of over 30 minutes/week more physical activity than those from Alabama (p=0.03 and p=0.02, respectively). The number of co-morbidities was found to be significantly associated with level of physical activity (p=0.02), where each additional comorbidity was associated with a mean decrease of 4.9 minutes/week of physical activity.
Table 4.
Multivariate model of variables associated with minutes of moderate/vigorous physical activity
| Variable | Beta Coefficient* |
Standard Error |
p value |
|---|---|---|---|
| Body mass index | −2.4 | 1.1 | 0.03 |
| Menopause status | |||
| Postmenopausal vs Pre or perimenopausal | −18.0 | 15.5 | 0.25 |
| Breast cancer stage | |||
| Stage II vs Stage I | −19.4 | 12.6 | 0.12 |
| Stage III vs Stage I | −29.4 | 16.5 | 0.08 |
| Cancer treatment | |||
| Both chemo and radiation vs neither | −21.1 | 19.7 | 0.28 |
| Chemo only vs neither | −21.2 | 21.3 | 0.32 |
| Radiation only vs neither | −30.9 | 21.9 | 0.16 |
| Clinical site | |||
| California versus Alabama | 34.3 | 15.3 | 0.03 |
| Colorado versus Alabama | 37.8 | 15.5 | 0.02 |
| Missouri versus Alabama | 19.5 | 15.7 | 0.22 |
| Hospitalizations | 2.8 | 7.9 | 0.73 |
| Emergency room visits vs none | −29.4 | 14.0 | 0.04 |
| Co-morbidities | −11.2 | 4.9 | 0.02 |
Beta coefficients are equivalent to weekly minutes of moderate/vigorous physical activity compared with the reference category for categorical variables, or per unit increase for continuous measures.
Discussion
Results of this study indicate that the majority of overweight or obese breast cancer survivors do not meet current physical activity guidelines and recommendations. As expected, fitness level and BMI were strongly associated with amount of physical activity reported, where there were higher levels of physical activity reported among those with higher levels of fitness and lower BMI. The number of co-morbidities was significantly and inversely associated with level of physical activity. Independent of other potentially influencing factors, the clinical site also was strongly associated with level of physical activity, which may reflect general regional differences in the culture and lifestyle in these areas. In this large heterogeneous sample, demographic characteristics, such as age, ethnicity, and education, and whether or not the participant received chemotherapy, were not significantly associated with whether or not participants met physical activity guidelines.
Previous studies that have examined potential determinants of physical activity in breast cancer survivors have involved various samples and time points in the cancer continuum. Determinants of exercise adherence during initial treatment (e.g., chemotherapy) and the immediate post-treatment period have been examined in two studies [16,17], but influencing factors during that time would be expected to be quite different than during survivorship, the time frame of the present study. Results from a 5-year longitudinal study of physical activity in stage II or III breast cancer suggest a natural trajectory following diagnosis and treatment, increasing gradually during the first 18 months (during recovery) and then declining steadily over the subsequent 42 months [15]. Time since diagnosis was not identified as being predictive of level of physical activity in our study, but the majority of the sample were more than 2 years post-diagnosis.
Results of two previous studies of physical activity in breast cancer survivors involved samples similar to that of the present study. One study analyzed the exercise habits of 806 women in the third year after their diagnosis enrolled in the Health, Eating, Activity, and Lifestyle (HEAL) Study [12,13]. In that cohort, BMI was significantly and inversely associated with level of physical activity. They found a significant inverse relationship between age and exercise where women ≥60 years old spent 44% less time in physical activity compared to women under 50 years of age. Disease stage was also significantly associated, where those with higher disease stages tended to exercise more than those with lower disease stages. That study also found that non-Hispanic white and Hispanic cancer survivors exercised more than black cancer survivors.
Another study involving 2819 breast cancer survivors enrolled in the Women’s Healthy Eating and Living (WHEL) study had similar results [14]. As in the HEAL study, the WHEL study found that black cancer survivors were likely to exercise less than non-Hispanic whites. However, age was not found to be significantly associated with physical activity level. Also, they found an inverse relationship between exercise and disease stage. Further, survivors who received only radiation treatment reported significantly higher amounts of exercise as compared to the survivors who received chemotherapy or a combination of radiation and chemotherapy. Time since diagnosis was not found to be significantly associated with level of physical activity, as in the present study. In the WHEL Study, education and diet composition were found to be significantly related to the amount of physical activity.
In the present study, we found a significant relationship between the number of co-morbidities and level of physical activity, and this was not examined in the WHEL and HEAL studies. In another WHEL study analysis, the presence of co-morbidities was found to affect outcomes, with type 2 diabetes mellitus significantly associated with reduced overall survival regardless of treatment group assignment [21]. The association between reduced physical activity and co-morbidities may be one factor that contributes to poorer outcome with co-morbidities. The ACSM guidelines for cancer survivors recommend that exercise prescriptions be individualized according to a cancer survivor’s medical co-morbidities, as well as pretreatment fitness and treatment-related side effects [11].
Also, the geographic location of the clinic site was found to be independently associated with level of physical activity. According to the Centers for Disease Control and Prevention (CDC) [22], Alabama has the highest prevalence of obesity, followed by Missouri, California and Colorado, among the regions of the clinical sites in this study. Although it may be expected that women in the regions with higher obesity rates would have lower amounts of physical activity, the clinical site remained significantly associated with physical activity level even after adjusting for BMI in the multivariate analysis. Notably, the order of lowest to highest level of physical activity by state in our multivariate model exactly matches the order in the CDC’s State Indicator Report on Physical Activity [23]. One hypothesis to explain this observation is that the general culture of the region may play a role such that, regardless of an individual’s degree of adiposity, the attitudes and general lifestyle of the region may not encourage physical activity among cancer survivors. This suggests that promotion of physical activity in the general population may benefit survivors across various geographic regions. Regional barriers associated with climate and walkability (hot, humid environments and roads that lack shoulders or sidewalks) may also explain this observation. Courneya et al. [17] found differential adherence to a supervised exercise intervention during breast cancer chemotherapy across site locations, although there were differences in the exercise facilities at these sites as well as climate and other regional factors.
In the general population, 48% of all adults living in the U.S. currently meet the physical activity guidelines set by the US DHHS. Further, 42.6% of all women living in the U.S. meet US DHHS guidelines [24]. Among the participants in the ENERGY study, less than 30% met these guidelines at enrollment. In the HEAL study, 32% of women met the recommendation of 150 min/week of any type of moderate- to vigorous-intensity physical activity when physical activity was defined as sports/recreational physical activity excluding household and yard work. Notably, however, when the HEAL study included activities such as household work and yard work, the percent of participants meeting the guidelines rose to 73% [13]. Across these previous studies and the present study, the evidence suggests that breast cancer survivors may benefit by more purposeful encouragement from their physicians with regard to physical activity.
There were several limitations in this study. In a cross-sectional analysis, it is recognized that the associated factors could be both the cause and effect of low level of physical activity. The participants were predominantly non-Hispanic white, and other racial and ethnic groups were not highly represented in our sample. Also, income levels, occupation, history of depression, access to health care, and dietary habits were not analyzed in this study. The self-reported nature of much of the physical activity data is also a limitation, because it is known that study participants often over-report their levels of physical activity [25].
In conclusion, the majority of overweight or obese breast cancer survivors entering a weight loss study do not meet current guidelines for physical activity. Degree of obesity, as well as regional differences and medical characteristics, appear to independently contribute to the likelihood of meeting current guidelines. The majority of overweight breast cancer survivors should be encouraged to increase their level of physical activity. Results from this study may help oncologists and primary care physicians develop educational and intervention programs and to prescribe exercise based on specific patient characteristics. Individualizing exercise prescriptions according to medical co-morbidities may improve adherence.
Acknowledgments
This ENERGY study was supported by National Cancer Institute Grant CA148791. The ENERGY Trial Group investigators: University of California, San Diego: Cheryl Rock, PhD, RD, Bilgé Pakiz, EdD, Barbara Parker, MD; University of California, Los Angeles: Patricia Ganz, MD; University of Colorado Anschutz Medical Campus, Aurora: Tim Byers, MD, MPH, Rebecca Sedjo, PhD, Holly Wyatt, MD, Anthony Elias, MD, James Hill, PhD; Washington University in St. Louis: Graham Colditz, MD, Kathleen Wolin, ScD, Jingxia Liu, PhD, Michael Naughton, MD; and University of Alabama at Birmingham: Wendy Demark-Wahnefried, PhD, RD, Helen Krontiras, MD, Maria Azrad, PhD, RD, Cindy Blair, PhD.
This project was also partially supported by the National Institutes of Health, grants TL1TR00098, CA23100, TR001082, and RR024992. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH.
Footnotes
Conflict of Interest
Conflict of Interest: Kathleen Wolin has equity in a digital health company whose products include weight management tools. All other authors declare that they have no conflict of interest. Cheryl Rock (corresponding author) and Shirley Flatt have full control of all primary data.
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