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© 2001 American Society for Clinical Oncology Changes in Weight, Body Composition, and Factors Influencing Energy Balance Among Premenopausal Breast Cancer Patients Receiving Adjuvant ChemotherapyFrom the Duke University Medical Center, Durham, NC; Department of Medicine, Harvard Medical School and Dana-Farber Cancer Institute, Boston, MA; and Division of Cancer Control and Population Sciences, National Cancer Institute, Bethesda, MD. Address reprint requests to Wendy Demark-Wahnefried, PhD, RD, LDN, Associate Research Professor of Surgery, Box 2619, Duke University Medical Center, Durham, NC 27710; email: demar001{at}mc.duke.edu
PURPOSE: Weight gain is a common problem among breast cancer patients who receive adjuvant chemotherapy (CT). We undertook a study to determine the causes of this energy imbalance. PATIENTS AND METHODS: Factors related to energy balance were assessed at baseline (within 3 weeks of diagnosis) and throughout 1 year postdiagnosis among 53 premenopausal women with operable breast carcinoma. Thirty-six patients received CT and 17 received only localized treatment (LT). Measures included body composition (dual energy x-ray absorptiometry), resting energy expenditure (REE; indirect calorimetry), dietary intake (2-day dietary recalls and food frequency questionnaires) and physical activity (physical activity records). RESULTS: Mean weight gain in the LT patients was 1.0 kg versus 2.1 kg in the CT group (P = .02). No significant differences between groups in trend over time were observed for REE and energy intake; however, a significant difference was noted for physical activity (P = .01). Several differences between groups in 1-year change scores were detected. The mean change (± SE) in LT versus CT groups and P values for uncontrolled/controlled (age, race, radiation therapy, baseline body mass index, and end point under consideration) analysis are as follows: percentage of body fat (-0.1 ± 0.4 v +2.2 ± 0.6%; P = .001/0.04); fat mass (+0.1 ± 0.3 v +2.3 ± 0.7 kg; P = .002/0.04); lean body mass (+0.8 ± 0.2 v -0.4 ± 0.3 kg; P = .02/0.30); and leg lean mass (+0.5 ± 0.1 v -0.2 ± 0.1 kg; P = .01/0.11). CONCLUSION: These data do not support overeating as a cause of weight gain among breast cancer patients who receive CT. The data suggest, however, that CT-induced weight gain is distinctive and indicative of sarcopenic obesity (weight gain in the presence of lean tissue loss or absence of lean tissue gain). The development of sarcopenic obesity with evidence of reduced physical activity supports the need for interventions focused on exercise, especially resistance training in the lower body, to prevent weight gain.
WEIGHT GAIN IS a common problem among patients with breast cancer who receive adjuvant chemotherapy (CT).1-5 This observation, first made by Dixon et al6 in 1978, was surprising because of the nausea, vomiting, and mucositis associated with CT.1,2,6 This finding was unexpected initially, but it has been reported consistently for more than two decades. Previous studies suggest that weight gain is especially pronounced among premenopausal women and among those who receive multiagent regimens.1,2 Weight gain commonly ranges from 2.5 to 6.2 kg; however, greater gains are not unusual.1,2 Boyd7 reported that 25% of premenopausal breast cancer patients gained more than 11 kg during the course of CT. Except in unusual cases, weight gain in women with breast cancer is undesirable for several reasons. First, it may negatively affect quality of life, because previous reports cite weight gain as "distressing" and a major concern within the patient population.3,4,8-12 Second, weight gain may predispose women to weight-related disorders such as hypertension, cardiovascular and gallbladder disease, orthopedic disturbances, and diabetes.13,14 Finally, although not conclusive, weight gain may adversely affect the risk of breast cancer recurrence.8,15,16 Camoriano et al8 observed 646 breast cancer patients for a median of 6.6 years and found that premenopausal patients who gained more than the median amount of weight (5.9 kg) were 1.5 times more likely to relapse and 1.6 times more likely to die of their breast cancer than women who gained less. Studies conducted by Chlebowski et al15 and Goodwin et al16 parallel these findings and argue for interventions that prevent weight gain during treatment, rather than the initiation of weight loss interventions after treatment. On the surface, the prevention of weight gain seems straightforward, and some trials have been launched based on the premise that this weight gain is a direct result of overeating. In a controlled, randomized trial of 104 early-stage breast cancer patients, Loprinzi et al17 found that breast cancer patients who received intensive diet counseling on energy-restricted diets did not gain significantly less weight than those assigned to the control arm. The lack of benefit from dietary counseling may have resulted from the fact that other components of energy balance, such as reduced physical activity, may play a greater role in weight gain than overeating. Thus, a clear understanding of the mechanisms that underlie CT-related weight gain is necessary to develop interventions that can most effectively prevent this common side effect.1,2 Only seven prospective studies have been reported that were designed to explore causes of CT-induced weight gain.18-24 Research efforts may be limited by the expense and time-intensive nature of such study, as well as the substantial patient burden. To date, studies have had several limitations: modest size, ranging from 8 to 38 subjects; brief duration, in which patients are monitored only during CT; and limited scope, in which one or two end points are assessed such as body composition or dietary intake, rather than the full complement of variables that contribute to energy balance. In addition, most of these studies relied on pre- and posttreatment data collected only for patients who received CT. Only one study, by Kutynec et al24 (N = 18) used breast cancer control patients who received only localized treatment (LT); this is a necessary component within the design to assess whether changes result from breast cancer CT or the disease. We report herein the results of a prospective trial designed to assess changes in dietary intake, resting energy expenditure (REE; caloric requirement to sustain basal metabolism), physical activity, and body composition that occur during the year after diagnosis of breast carcinoma in premenopausal women. To assess the impact of systemic CT, two groups of patients were enrolled and compared: those who received systemic CT and local management (surgery with or without radiation therapy [XRT]) versus patients who did not receive CT and who received only LT. With data on 53 patients, this research effort represents the largest, most comprehensive, and longest-term study of its kind to date.
Eligibility, Recruitment, and Enrollment Women with newly diagnosed, operable breast carcinoma were identified from the Breast Program at the Duke Comprehensive Cancer Center (Durham, NC) or were referred by community-based physicians. Subjects were required to be euthyroid without thyroid medication, without serious comorbid conditions or conditions that would affect body composition (eg, paralysis, amputation, and so forth), mentally competent, and able to speak English. In addition, only premenopausal patients (defined as < 4 months since the last menstrual period and/or follicle-stimulating hormone level in the premenopausal range) were screened for enrollment, because previous studies suggest that weight gain is greater and more problematic in this population.1,2,4,5,8 Only patients whose treatment was confined to local management alone (surgery with or without XRT) or those who received CT in addition to local management were eligible. Because hormonal agents such as tamoxifen and megestrol acetate have been associated with weight gain, patients who were to receive hormonal therapies as sole systemic treatment were excluded.25,26 Patients were contacted within 3 weeks of surgery (mastectomy or lumpectomy) and before the initiation of adjuvant treatment. The protocol was approved by the institutional review board at Duke University Medical Center, and signed consent was obtained from all patients who agreed to participate. Participants were reimbursed for mileage and also were given a $25 monetary incentive to help defray the costs of participation.
Measures and Measurement Points
Dietary Intake Because dietary intake is a key component of energy balance, and methods to assess food consumption have inherent biases, dietary intake was assessed using two different methods: (1) dietary recalls; and (2) food frequency questionnaires (FFQs). Multiple pass 2-day dietary recalls. Dietary recalls were conducted at baseline, on a monthly basis for the first 6 months, and on a bimonthly basis for the remainder of the study period. Two random, unannounced, telephone-administered dietary recalls of 1 weekday and 1 weekend day were conducted and averaged for each time point. Recalls were conducted by a trained nutritionist with the multiple-pass technique, in which the interviewer queries the respondent repeatedly to garner detailed and complete information regarding the participant’s food intake during the preceding 24 hours, including portion-size information, food preparation methods, specific brand item use, and the use of condiments. This technique was selected specifically because it decreases the extent of underreporting and renders data comparable to doubly labeled water, the gold standard.27 Dietary intakes were entered and analyzed for energy content and other nutrients using the Minnesota Nutrition Data System developed at the University of Minnesota (St. Paul, MN). Output analyses were reviewed for out-of-field observations and completeness. FFQ. The optically scannable 116-item FFQ, developed at the Fred Hutchinson Cancer Research Center (Seattle, WA),28 was administered at baseline, 6 months, and 1 year. This validated instrument has been used in several epidemiologic, cross-sectional, and interventional studies.29-31 Participants were asked to complete the survey "thinking back on their usual food intake during the past 6 months." FFQs were reviewed for stray marks, incomplete data, and failed logic checks; forms were analyzed by the Fred Hutchinson Cancer Research Center and data were merged with existing data sets.
Physical Activity
REE
Body Composition
Height/Weight
Menstrual Record
Power Calculations/Statistical Analysis Within each group, the distribution of all dependent variables was unimodal, and most distributions were not skewed. Baseline characteristics of the two groups were compared with Fisher’s exact test and the t test. Mixed linear models with compound symmetry covariance structures were used to test the difference between the two groups in trend across time on the dependent variables. For each dependent variable, both unadjusted and covariate-adjusted tests of trend were tested. The covariates included race (white v other), age, whether the patient received XRT, body mass index (BMI) at baseline, and baseline value of the dependent variable under consideration. Unadjusted group effects were summarized with means and SEs across time. A two-sided Type I error rate of 0.05 was used throughout data analysis.
Sample Characteristics From January 27, 1995 to February 22, 1999, 122 eligible patients were approached to participate; of these, 60 women gave signed consent. There were no significant differences between participants and nonparticipants with regard to age, race, or BMI; however, the acceptance rate was significantly higher among patients in the CT group versus the LT group (54% v 42%, respectively; P < .05). The overwhelming stated reason for refusal in more than 97% of cases was "lack of time." Figure 1 shows the study flow with dropouts and participants who were subsequently discontinued from follow-up because they did not meet eligibility criteria. We excluded the data of one LT group participant who quit smoking immediately after accrual and gained 9.8 kg. She was the only smoker in the sample, and given the strong, independent association between weight gain and smoking cessation, these data were not included in the analysis.36 Demographic and treatment-related characteristics of the resultant study population are summarized in Table 1.
At baseline, no differences were detected between LT and CT group women with regard to age, race, and height (Table 1). Women in the CT group had significantly later-stage disease, however, and they were more likely to receive XRT. It addition, women in the CT group were significantly heavier and had higher amounts of both body fat and lean tissue, as well as higher proportional body fat percentages, compared with patients in the LT group. Women in the CT group also were more likely to develop amenorrhea, which was sustained throughout the study period.
Energy Intake
REE REE over time is shown in Fig 3. Although the curve for the CT group is clearly higher across all time points, this was expected given the greater body size and lean body mass of this group. Aside from this distinction, no difference between groups in the linear trend across time was noted. This finding persisted regardless of how REE was expressed (eg, REE, REE as a function of lean body mass or total body mass, or REE as a function of predicted REE).
Physical Activity Energy Expenditure Energy demands for physical activity are plotted in Fig 4. A significant difference in the unadjusted quadratic trend across time was noted between groups (P = .01); after covariate-adjusted tests, P = .16.
Body Composition Changes in body weight and composition during the 1-year study period are listed in Table 2. Differences between groups in linear trend across time were noted for several variables in uncontrolled analyses (body weight, BMI, percentage of body fat, fat mass, lean body mass, and leg lean mass). After analyses were controlled for age, race, XRT, and values for baseline BMI and the parameter studied, P values for body weight, BMI, lean body mass, and leg mean mass exceeded an alpha of 0.05, but they still provided evidence of a trend. In general, our data demonstrate that during the course of the study year, women in the LT group had a stable fat mass, slight decreases in percentage of body fat, and slight increases in total and leg lean body mass. In contrast, women in the CT group experienced increases in fat mass and percentage of body fat and decreases in leg lean body mass. Changes in lean body and fat mass during the study period for both groups are graphed in Fig 5.
CT-induced weight gain has been an unexplained problem for decades.1,2 Although this energy imbalance has been the attributed to overeating, there is a dearth of solid data to support this conclusion. Data from this study, in which dietary data were collected using two different methodologies, do not support overeating as a cause. These findings are consistent with four of the five prospective studies conducted to date that have used validated dietary data collection methods.20-24 Despite the accumulation of evidence, however, the limits of the methodology mean that the possibility of increased energy intake as a modest contributor to weight gain still cannot be excluded. To determine primary factors that contribute to weight gain, focus shifts to the possibility of decreased energy expenditure via reductions in physical activity and/or REE. Unlike our previous study, in which decreases in REE were detected midtreatment among breast cancer patients receiving CT, data from this study failed to detect differences between groups over time.21 This discrepancy may have occurred because we did not measure REE at the same time points. An additional explanation is that patients in our previous study lost lean body mass but were weight stable, whereas patients in this study also lost lean body mass but gained significant amounts of fat. Although muscle is more metabolically active than fat, fat is not inert and it requires energy for support. Thus, it is possible that no metabolic differences were seen with the net loss of 0.4 kg of lean body mass, because effects would have been masked by the net gain of 2.3 kg of fat. Therefore, our data more closely mirror those of Foltz22 and Kutynec et al,24 who also did not find metabolic changes. In this study, decreased physical activity seems to be the most likely factor that contributes to positive energy balance. These findings are in contrast to those of Kutynec et al24 (N = 17) and Foltz22 (N = 34), who did not detect decreases in physical activity by use of the Ainsworth et al37 Compendium of Physical Activity, or the Wage-Earner and Housekeeping Scales of the Psychiatric Status Schedule,38 respectively. Small sample sizes or insensitive methods are possible reasons that no differences were found in these two studies. The current data, however, support the data from our previous investigation, in which we also found decreased levels of physical activity throughout treatment, from a baseline level of 514 ± 117 kcal per day to an average of 461 ± 83 kcal per day during the course of therapy (N = 18).21 Our findings also support those of Rock et al,39 who conducted a cross-sectional study of breast cancer survivors and found that routine physical activity was the strongest predictor of weight stability. Finally, our data support the findings of Goodwin et al,40 who performed a diet-exercise intervention and found strong associations between weight stability and physical activity, but little association with caloric restriction. The most compelling data from this study relate to observed changes in body composition. Five previous studies that have assessed body composition prospectively after breast cancer diagnosis, as well as our data, demonstrate that CT-induced weight gain is atypical.18-21,24 Typical weight gain is characterized by increases in both lean body mass and adipose tissue, and lean tissue comprises 29% to 43.6% of each pound gained.41 However, CT-induced weight gain seems to occur either in the absence of gains in lean tissue or in the presence of lean tissue losses. Furthermore, our study used dual-energy x-ray absorptiometry to characterize changes in body composition in specific body zones such as the legs, trunk, and arms; our data support previous findings that lean body losses occur predominantly in the legs and lower trunk.24 These data support previous observations that breast cancer patients who receive CT develop sarcopenic obesity, ie, weight gain without concurrent gains in lean body mass.42 Acute sarcopenic obesity is uncommon, and it typically is observed with the chronic use of corticosteroids, hypopituitarism, specific neuromuscular diseases, hypogonadism, and prolonged physical inactivity or bed rest.42 Gradual sarcopenic obesity is noted with increased age and menopause.43 Because all women in the CT group developed amenorrhea, an effect that was sustained throughout the study period in most, premature menopause may be partly responsible for these observed changes. Unfortunately, this study was not designed to determine whether menopausal onset could explain either differences in body composition or factors that influence energy metabolism. Therefore, analyses were not undertaken to explore this issue because such analyses would be severely underpowered. Results of a prospective study of locoregional breast cancer patients by Goodwin et al,4 however, suggest that the onset of menopause and the administration of CT were the sole independent predictors of weight gain in both univariate and multivariate analyses; premenopausal patients (N = 305) who remained premenopausal gained only 0.7 kg (95% CI, 0.4 to 1.8 kg), whereas those who became postmenopausal gained 2.7 kg (95% CI, 1.7 to 3.6 kg; P = .002). A comparison of data from our breast cancer patients who received CT with those of healthy women enrolled in the Fels Longitudinal Study43 reveals similarities at baseline; mean percentages of body fat for the average 40-year-old American woman and the average 41-year-old woman in our CT group are 33.5 ± 8.3% and 33.6 ± 8.6%, respectively. Therefore, our data do not support an association between sarcopenic obesity and breast cancer risk as reported previously by Heber et al.42 Within the span of only 1 year, however, the patient who receives CT achieves a body fat percentage of 35.8 ± 8.9%; the average American woman would not achieve this body fat percentage until age 50 years, which roughly corresponds to the age for menopause.43 Changes in body composition characteristic of normal aging clearly are accelerated in patients who receive CT, and most of these changes occur within 6 months of diagnosis. In contrast, women in the LT group experienced slight improvements in body composition. Within this group, however, significantly fewer patients developed sustained amenorrhea. Physical activity, especially resistance training, represents the cornerstone of treatment for sarcopenic obesity.42 Exercise interventions and strength training directed toward the leg region may be particularly useful, because data from this study and that of Kutynec et al24 suggest that greater losses of lean tissue occur in this region. To date, physical activity interventions directed toward breast cancer patients have concentrated largely on the potential of aerobic exercise to reduce nausea and fatigue and improve quality of life.44-47 It is possible, however, that combined programs of aerobic and strength training exercise may convey even greater and more far-reaching benefits. Although this study is the largest of its kind, and we used validated methods for data collection, it still was limited by its modest sample size and methods that may have been insensitive for the detection of subtle changes in factors related to energy metabolism. Future studies that are longer in duration, that have larger sample sizes, and that use methods such as doubly-labeled water would enhance our understanding of CT-induced energy imbalance. Future research also should be designed for consideration of the following issues: (1) the value of a nonsystemic control group (although shifting practice patterns with regard to tamoxifen may make implementation difficult); and (2) appropriate control for potential body mass differences at baseline between LT and CT groups. Although we controlled for baseline body mass in our analyses, we were surprised to observe significant differences at baseline. Certainly, given the strong association between stage and treatment, we expected to observe stage differences between groups. We also appreciated previous studies that reported positive associations between body weight and later stage at diagnosis and/or disease progression.1,2,48 Given the modest size of this study, however, we did not expect to find significant differences with respect to body mass, adiposity, and/or musculature at baseline, and these differences were striking. Therefore, these data lend further support to the association between disease progression and increased body weight, which may be driven by underlying growth factors and hormonal levels.49 Our study is the largest and longest prospective study conducted to date to compare body composition changes and factors associated with energy balance among patients with operable breast carcinoma who received CT versus those treated with LT only. The data confirm the consistent observation of five previous studies, which demonstrated that CT-induced weight gain occurs either in the absence of lean tissue gain or in the presence of lean tissue loss characteristic of sarcopenic obesity.18-22,24 This study also was the second to suggest that decreased physical activity may be a factor that contributes to positive energy balance.21 These findings provide valuable information for the development of interventions to curb deleterious changes in body composition and weight gain, and they support a need to develop interventions that get breast cancer patients moving.50 Evaluation of such interventions also will refine our knowledge of the fundamental mechanisms that underlie CT-induced weight gain.
Supported by grant no. 1K07-CA62215 from the National Cancer Institute. We thank the following individuals who were instrumental in facilitating this research: Shelley Alvey; Karen Brunatti, RN; Michael Carpenter, MS; O. Michael Colvin, MD; Cheryl Franklin-Cook; David Coniglio, PA; Dana Fifield, RN; Gregory Georgiade, MD; Patricia Hardenbergh, MD; Lyndsay Harris, MD; Kathleen Havlin, MD; Barbara Horne, RN; J. Dirk Iglehart, MD; Nancy Langman; George Leight, MD; Herbert K. Lyerly, MD; Rex McCallum, MD; Gregory McElveen; MS; Leonard Prosnitz, MD; Scott Pruitt, MD; Patsy Smitheran, PA; Wilma Stanley; Linda Sutton, MD; Sherri Westbrook; and Cheri Willard. Most of all, we are indebted to the women who participated in this research.
1. Demark-Wahnefried W, Rimer BK, Winer EP: Weight gain in women diagnosed with breast cancer. J Am Diet Assoc 97: 519-529, 1997[Medline]
2.
Demark-Wahnefried W, Winer EP, Rimer BK: Why women gain weight with adjuvant chemotherapy for breast cancer. J Clin Oncol 11: 1418-1429, 1993 3. Ganz PA, Schag CC, Polinsky ML: Rehabilitation needs and breast cancer: The first month after primary therapy. Breast Cancer Res Treat 10: 243-253, 1987[Medline]
4.
Goodwin PJ, Ennis M, Pritchard KI, et al: Adjuvant treatment and onset of menopause predict weight gain after breast cancer diagnosis. J Clin Oncol 17: 120-129, 1999 5. Heasman KZ, Sutherland HJ, Campbell JA, et al: Weight gain during adjuvant chemotherapy for breast cancer. Breast Cancer Res Treat 5: 195-200, 1985[Medline] 6. Dixon J, Moritz D, Baker F: Breast cancer and weight gain: An unexpected finding. Oncol Nurs Forum 5: 5-7, 1978
7.
Boyd NF: Nutrition and breast cancer. J Natl Cancer Inst 85: 6-7, 1993 8. Camoriano JK, Loprinzi CL, Ingle JN, et al: Weight change in women treated with adjuvant therapy or observed following mastectomy for node-positive breast cancer. J Clin Oncol 8: 1327-1334, 1990[Abstract] 9. Knobf MK, Mullen JC, Xistris D, et al: Weight gain in women with breast cancer receiving adjuvant chemotherapy. Oncol Nurs Forum 10: 28-34, 1983
10.
Kornblith AB, Hollis DR, Zuckerman E, et al: Effect of megestrol acetate on quality of life in a dose-response trial in women with advanced breast cancer. J Clin Oncol 11: 2081-2089, 1993 11. Levine EG, Raczynski JM, Carpenter JT: Weight gain with breast cancer adjuvant treatment. Cancer 67: 1954-1959, 1991[Medline] 12. Monnin S, Schiller MR, Sachs L, et al: Nutritional concerns of women with breast cancer. J Cancer Edu 8: 63-89, 1993[Medline]
13.
Brown BW, Brauner C, Minnotte MC: Noncancer deaths in white adult cancer patients. J Natl Cancer Inst 85: 979-997, 1993 14. Li FP, Stovall E: Long-term survivors of cancer. Cancer Epidemiol Biomarkers Prev 7: 269-270, 1998[Medline] 15. Chlebowski RT, Weiner JM, Reynolds R, et al: Long-term survival following relapse after 5-FU but not CMF adjuvant breast cancer therapy. Breast Cancer Res Treat 7: 23-29, 1986[Medline] 16. Goodwin PA, Panzarella T, Boyd NF: Weight gain in women with localized breast cancer: A descriptive study. Breast Cancer Res Treat 11: 59-66, 1988[Medline] 17. Loprinzi CL, Athmann LM, Kardinal CG, et al: Randomized trial of dietician counseling to try to prevent weight gain associated with breast cancer adjuvant chemotherapy. Oncology 53: 228-232, 1996[Medline] 18. Aslani A, Smith RC, Allen BJ, et al: Changes in body composition during adjuvant chemotherapy for breast cancer. Applied Radiation Isotopes 49: 637-638, 1998 19. Aslani A, Smith RC, Allen BJ, et al: Changes in body composition during breast cancer chemotherapy with the CMF-regimen. Breast Cancer Res Treat 57: 285-290, 1999[Medline]
20.
Cheney CL, Mahloch J, Freeny P: Computerized tomography assessment of women with weight changes associated with adjuvant treatment for breast cancer. Am J Clin Nutr 66: 141-146, 1997
21.
Demark-Wahnefried W, Hars V, Conaway MR, et al: Reduced rates of metabolism and decreased physical activity in breast cancer patients receiving adjuvant chemotherapy. Am J Clin Nutr 65: 1495-1501, 1997 22. Foltz AT: Weight gain among stage II breast cancer patients: A study of five factors. Oncol Nurs Forum 12: 21-26, 1985 23. Grindel CG, Cahill CA, Walker M: Food intake of women with breast cancer during their first six months of chemotherapy. Oncol Nurs Forum 16: 401-407, 1989[Medline] 24. Kutynec CL, McCargar L, Barr SI, et al: Energy balance in women with breast cancer during adjuvant chemotherapy. J Am Diet Assoc 99: 1222-1227, 1999[Medline] 25. Hoskin PJ, Ashley S, Yarnold JR: Weight gain after primary surgery for breast cancer: Effect of tamoxifen. Breast Cancer Res Treat 22: 129-132, 1992[Medline]
26.
Loprinzi CL, Kugler JW, Sloan JA, et al: Randomized comparison of megestrol acetate versus dexamethasone versus fluoxymesterone for the treatment of cancer anorexia/cachexia. J Clin Oncol 17: 3299-3306, 1999 27. Johnson RK, Driscoll P, Goran MI: Comparison of multiple-pass 24-hour recall estimates of energy intake with total energy expenditure determined by doubly labeled water method in young children. J Am Diet Assoc 96: 1140-1144, 1996[Medline]
28.
Kristal A, Feng Z, Coates R, et al: Associations of race, ethnicity, education and dietary intervention on validity and reliability of a food frequency questionnaire in the Women’s Health Initiative Feasibility Study in Minority Populations. Am J Epidemiol 146: 856-869, 1997 29. Glanz K, Kristal AR, Tilley BC, et al: Psychosocial correlates of healthful diets among male auto workers. Cancer Epidemiol Biomarkers Prev 7: 119-126, 1998[Abstract]
30.
Coates RJ, Bowen DJ, Kristal AR, et al: The Women’s Health Trial Feasibility Study in Minority Populations: Changes in dietary intakes. Am J Epidemiol 149: 1104-1112, 1999
31.
Cohen J, Kristal A, Stanford J: Fruit and vegetable intakes and prostate cancer risk. J Natl Cancer Inst 92: 61-68, 2000 32. Sallis J, Haskell W, Wood P, et al: Physical activity assessment methodology in the Five-City Project. Am J Epidemiol 21: 91-106, 1985
33.
Simonson D, DeFronzo R: Indirect calorimetry: Methodological and interpretative problems. Am J Physiol 258: E399-412, 1990 34. Weir JB: New methods for calculating metabolic rate with special reference to protein metabolism. J Physiol 109: 1-9, 1949 35. Gordon CG, Chumlea WC, Roche AF: Stature, recumbent length, and weight, in Lohman TG, Roche AF, Martorell F (eds): Anthropometric Standardization Reference Manual. Champaign IL, Human Kinetics, 1988, pp 3-8
36.
O’Hara P, Connett JE, Lee WW, et al: Early and late weight gain following smoking cessation in the Lung Health Study. Am J Epidemiol 148: 821-830, 1998 37. Ainsworth BE, Haskell WL, Leon AS, et al: Compendium of physical activities: Classification of energy costs of human physical activities. Med Sci Sports Exerc 25: 71-80, 1993[Medline]
38.
Silberfarb P: Psychological aspects of neoplastic disease. Am J Psychiatry 137: 450-455, 1980 39. Rock CL, Flatt SW, Newman V, et al: Factors associated with weight gain in women after diagnosis of breast cancer: Women’s Healthy Eating and Living Study Group. J Am Diet Assoc 99: 1212-1221, 1999[Medline] 40. Goodwin P, Esplen MJ, Butler K, et al: Multidisciplinary weight management in locoregional breast cancer: Results of a phase II study. Breast Cancer Res Treat 48: 53-64, 1998[Medline] 41. Forbes GB, Brown MR, Welle SL, et al: Deliberate overfeeding in women and men: Energy cost and composition of weight gain. Br J Nutr 56: 1-9, 1986[Medline]
42.
Heber D, Ingles S, Ashley JM, et al: Clinical detection of sarcopenic obesity by bioelectrical impedance analysis. Am J Clin Nutr 64: 472S-477S, 1996 (suppl)
43.
Guo SS, Zeller C, Chumlea WC, et al: Aging, body composition, and lifestyle: The Fels Longitudinal Study. Am J Clin Nutr 70: 405-411, 1999 44. Courneya KS, Friedenreich CM: Physical exercise and quality of life following cancer diagnosis: A literature review. Ann Behav Med 21: 171-179, 1999[Medline] 45. Friedenreich CM, Courneya KS: Exercise as rehabilitation for cancer patients. J Sports Med 6: 237-242, 1996 46. Graydon J, Bubela N, Irvine D, et al: Fatigue-reducing strategies used for patients receiving treatment for cancer. Cancer Nurs 18: 23-28, 1995[Medline] 47. Winningham ML, MacVicar MG: The effect of aerobic exercise on patient reports of nausea. Oncol Nurs Forum 15: 447-450, 1988[Medline]
48.
Hunt KA, Sickles EA: Effect of obesity on screening mammography: Outcomes analysis of 88,346 consecutive examinations. AJR Am J Roentgenol 174: 1251-1255, 2000 49. Kaaks R: Nutrition, hormones, and breast cancer: Is insulin the missing link? Cancer Causes Control 7: 605-25, 1996[Medline]
50.
McTiernan A: Exercise and breast cancer: Time to get moving? N Engl J Med 336: 1311-1312, 1997. Submitted December 7, 2000; accepted January 5, 2001.
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Copyright © 2001 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
