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American Journal of Epidemiology Advance Access originally published online on December 7, 2005
American Journal of Epidemiology 2006 163(2):101-107; doi:10.1093/aje/kwj017
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American Journal of Epidemiology Copyright © 2005 by the Johns Hopkins Bloomberg School of Public Health All rights reserved; printed in U.S.A.

Original Contribution

Association of Overweight with Breast Cancer Survival

Meng-Hua Tao1,2, Xiao-Ou Shu1, Zhi Xian Ruan3, Yu-Tang Gao3 and Wei Zheng1

1 Department of Medicine, Center for Health Services Research, Vanderbilt-Ingram Cancer Center, Vanderbilt University, Nashville, TN
2 Department of Epidemiology, School of Public Health, University of California at Los Angeles, Los Angeles, CA
3 Department of Epidemiology, Shanghai Cancer Institute, Shanghai, China

Correspondence to Dr. Xiao-Ou Shu, Vanderbilt University Center for Health Services Research, Medical Center East, Suite 6000, Nashville, TN 37232-8300 (e-mail: Xiao-Ou.Shu{at}Vanderbilt.edu).

Received for publication May 13, 2005. Accepted for publication August 19, 2005.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
The authors investigated the association between overweight at the time of or soon after cancer diagnosis and survival in a cohort of 1,455 breast cancer patients aged 25–64 years. The patients were recruited into the Shanghai Breast Cancer Study (Shanghai, China), a population-based case-control study, between August 1996 and March 1998. The median follow-up time for this cohort was 5.1 years (1996–2002) after breast cancer diagnosis, and 240 deaths were identified. Being overweight at cancer diagnosis or soon afterward, as measured by body mass index (BMI; weight (kg)/height (m)2), was associated with poorer overall survival and disease-free survival. Five-year survival rates were 86.5%, 83.8%, and 80.1% for subjects whose BMIs were <23.0, 23.0–24.9, and ≥25.0, respectively (p = 0.02); the corresponding 5-year disease-free survival rates were 81.9%, 78.1%, and 76.6% (p = 0.05). The inverse association between BMI and survival persisted after adjustment for age at diagnosis and other known prognostic factors for breast cancer, including disease stage. The authors found neither waist:hip ratio nor waist circumference to be independently associated with overall survival or disease-free survival. These results suggest that excess weight may be an independent predictor of breast cancer survival among Chinese women.

body mass index; body weight; breast neoplasms; mortality; survival; waist-hip ratio

Abbreviations: BMI, body mass index; CI, confidence interval; ER, estrogen receptor; HR, hazard ratio; PR, progesterone receptor; TNM, tumor-node-metastasis


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Research has suggested that obesity is associated with increased risk of breast cancer among postmenopausal women but is unrelated or inversely related to risk among premenopausal women (1Go). The association between body size and breast cancer prognosis has been investigated in a number of studies, mainly studies conducted in Western countries (2Go–27Go). Increased body weight or body mass index (BMI; weight (kg)/height (m)2) has been found to be inversely associated with overall survival and disease-free survival in both pre- and postmenopausal women, although the evidence is not entirely consistent (28Go). The effect of body fat distribution on breast cancer prognosis has also been examined (13Go, 15Go, 23Go, 29Go). Elevated waist:hip ratio was associated with breast cancer mortality among postmenopausal women in one study (23Go) but not in another (13Go).

It has been suggested that Asian Americans have better survival rates for breast cancer than non-Hispanic Whites in the United States (30Go), and Asian women also typically have a low prevalence of overweight/obesity. However, the relation between overweight/obesity and survival after breast cancer diagnosis in Asians has only been evaluated in two small-scale studies (6Go, 31Go). In this report, we describe the association between being overweight at or soon after breast cancer diagnosis and breast cancer survival in a cohort of breast cancer patients recruited into the Shanghai Breast Cancer Study, a population-based case-control study.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
Subjects and study design
Through a rapid case-ascertainment system supplemented by the population-based Shanghai Cancer Registry, we identified 1,602 women aged 25–64 years who were diagnosed with primary breast cancer in Shanghai, China, between August 1996 and March 1998. Of these women, 1,459 (91.1 percent) completed an in-person interview and were included in the Shanghai Breast Cancer Study as cases. Reasons for nonparticipation included refusal (109 cases; 6.8 percent), death prior to interview (17 cases; 1.1 percent), and inability to locate potential subjects (17 cases; 1.1 percent).

Weight, waist and hip circumferences, and sitting and standing heights were measured in all study participants by trained interviewers according to a standard protocol. Two measurements were taken for each variable, with a tolerance of less than 1 cm for height and waist and hip circumferences and a tolerance of 1 kg for weight. A third measurement was taken if the difference between the first two was larger than the tolerances stated above. The averages of the two closest measurements were used to calculate BMI and waist:hip ratio.

Two senior pathologists independently reviewed pathologic slides to confirm the initial cancer diagnoses. Information on cancer diagnosis, cancer stage (as measured by tumor-node-metastasis (TNM) stage), cancer treatment, and estrogen receptor (ER)/progesterone receptor (PR) status was abstracted from medical charts using a standard protocol.

Patients were followed through January 2003 with a combination of active follow-up and record linkage to death certificates kept by the Vital Statistics Unit of the Shanghai Municipal Center for Disease Control and Prevention. Of the 1,459 patients included in the original study, 1,290 (88.4 percent) patients or next of kin were successfully contacted either in person (n = 1,241; 85.0 percent) or by telephone (n = 49; 3.4 percent) between March 2000 and December 2002. Two hundred (15.5 percent) of the 1,290 patients were deceased. Through interviews with patients or (for deceased patients) next of kin, we obtained information on disease progress, recurrence, and (if deceased) cause of death. Survival status for the remaining 169 participants who could not be contacted through a home visit or by telephone was established in June 2003 by linkage to the death registry. Forty deaths were identified with this method, and information on the date and cause of death was obtained. There were 126 subjects for whom no match in the death registry could be found, and they were assumed to be still living. We assigned December 31, 2002—6 months prior to our search of the death registry—as the censoring date for these subjects in order to allow for a possible delay of entry of death certificates into the registry. Four subjects had insufficient information for record linkage and were excluded from the current analysis. This study was approved by the institutional review boards of all participating institutions.

Statistical analysis
The primary outcomes for this study were overall survival and disease-free survival. The endpoint for the analysis of overall survival was any death, and for the analysis of disease-free survival it was cancer recurrence/metastasis or death related to breast cancer. Survival time was calculated as the time from cancer diagnosis to the endpoints of the study, censoring at the date of last contact or noncancer death (for disease-free survival only). We used the Kaplan-Meier method to compute 5-year survival and 5-year disease-free survival rates, and we applied the log-rank test to evaluate the differences in survival across different strata. Quartile distributions were used to categorize data on BMI, waist:hip ratio, and waist circumference. We also constructed BMI and waist:hip ratio categories using the classification for Asians recommended by the World Health Organization (32Go). We checked the proportional hazards assumption through log plots. We applied the Cox regression model to evaluate the effect of BMI and waist:hip ratio on overall survival with adjustment for age at diagnosis (treated as a continuous variable) and other known prognostic factors for breast cancer. We further evaluated the associations of BMI and waist:hip ratio with the study outcomes by stratifying on TNM stage and menopausal status. Menopausal status was defined as no menstruation during the past 12 months, excluding those lapses caused by pregnancy or breastfeeding. All statistical tests were based on two-sided probability. Statistical analyses were conducted using SAS, version 9.1 (SAS Institute, Inc., Cary, North Carolina).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
During the study period, 240 of the 1,455 patients were found to be deceased, with an overall 5-year survival rate of 84.0 percent. Table 1 presents the associations of selected demographic factors and known breast cancer prognostic factors with overall 5-year survival rate. Women with breast cancer diagnosed at a younger age (<40 years) and during the perimenopausal period (ages 50–59 years) had a lower 5-year survival rate than women in other age groups. As expected, TNM stage was an important prognostic factor for overall survival. The majority of patients (99 percent) underwent surgery, and as part of their regular treatment for breast cancer, 94 percent of patients received adjuvant chemotherapy. Traditional Chinese medicine was also commonly used; 63.0 percent of patients received both adjuvant chemotherapy and traditional Chinese medicine. We did not have specific information on chemotherapy for each patient in this study; however, on the basis of data from an ongoing study of 2,245 breast cancer survivors in Shanghai, we estimated that 92 percent of the patients received adjuvant chemotherapy. Among these persons, 84 percent received 5-fluorouracil, 89 percent received cyclophosphamide, and 30 percent received methotrexate as part of their chemotherapy. Having received radiotherapy was associated with a lower overall survival rate; this may have been related to a late stage of disease at diagnosis. Information on tamoxifen use was obtained during the follow-up survey. As expected, patients treated with tamoxifen had a more favorable prognosis than nonusers and those without information. ER/PR status was not significantly associated with survival in this population. However, information on ER/PR status was missing for approximately 30 percent of subjects.


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  		TABLE 1. Overall survival of breast cancer patients according to demographic factors and known breast cancer prognostic factors, Shanghai Breast Cancer Study, Shanghai, China, 1996–2002

 
BMI at the time of interview was inversely associated with overall survival and disease-free survival (table 2). Five-year overall survival rates were 86.5 percent, 83.8 percent, and 80.1 percent for patients with BMIs of <23.0, 23.0–24.9, and ≥25.0, respectively (p = 0.02); the corresponding 5-year disease-free survival rates were 81.9 percent, 78.1 percent, and 76.6 percent (p = 0.05). Survival curves by BMI are shown in figures 1 and 2. Of the 240 deceased patients in our study, 218 (90.8 percent) died of breast cancer. We also conducted survival analyses for breast-cancer-specific mortality and found that the association between breast-cancer-specific mortality and BMI was similar to that reported for overall survival (data not shown). Waist circumference was significantly related to 5-year overall survival but not to disease-free survival. There were no significant differences in 5-year overall survival rates and disease-free survival rates across categories of waist:hip ratio.


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  		TABLE 2. Associations of body mass index,* waist:hip ratio, and waist circumference with 5-year overall survival and disease-free survival among breast cancer patients, Shanghai Breast Cancer Study, Shanghai, China, 1996–2002

 


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  		FIGURE 1. Five-year overall survival after diagnosis of breast cancer, by body mass index (weight (kg)/height (m)2), Shanghai Breast Cancer Study, Shanghai, China, 1996–2002. Triangles, body mass index <23.0; squares, body mass index 23.0–24.9; circles, body mass index ≥25.0.

 


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  		FIGURE 2. Five-year disease-free survival after diagnosis of breast cancer, by body mass index (weight (kg)/height (m)2), Shanghai Breast Cancer Study, Shanghai, China, 1996–2002. Triangles, body mass index <23.0; squares, body mass index 23.0–24.9; circles, body mass index ≥25.0.

 
Table 3 shows the associations of BMI, waist:hip ratio, and waist circumference with overall and disease-free survival after adjustment for age at diagnosis and other known prognostic factors for breast cancer. Patients in the highest quartile of BMI had significantly poorer overall survival and disease-free survival than patients in the lowest quartile (adjusted hazard ratio (HR) = 1.4 (95 percent confidence interval (CI): 1.0, 2.0) and adjusted HR = 1.3 (95 percent CI: 1.0, 1.8), respectively). Similarly, the adjusted hazard ratios associated with a BMI greater than or equal to 25 were 1.3 (95 percent CI: 1.0, 1.8) and 1.3 (95 percent CI: 1.0, 1.7) for overall and disease-free survival, respectively, in comparison with subjects of normal weight (BMI < 23.0). We found neither waist:hip ratio nor waist circumference to be associated with overall survival or disease-free survival in the multivariate analyses.


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  		TABLE 3. Relative hazards of mortality and disease progression after diagnosis of breast cancer, by body mass index,* waist:hip ratio, and waist circumference, Shanghai Breast Cancer Study, Shanghai, China, 1996–2002

 
The median interval between breast cancer diagnosis and interview for cases was 67 days (25th–75th percentiles, 3–137), and this interval did not appear to differ between obese and nonobese breast cancer patients. Additional adjustment for interval between disease diagnosis and interview, usual physical activity, and total energy intake 5 years prior to diagnosis did not appreciably change the risk estimates presented in table 3 (data not shown).

Postmenopausal women had poorer overall and disease-free survival rates than premenopausal women (adjusted HR = 1.9 (95 percent CI: 1.3, 2.9) and adjusted HR = 2.1 (95 percent CI: 1.5, 3.1), respectively). Among postmenopausal women, BMI was found to be associated with increased, though not significantly increased, risks of death (HR = 1.2 (95 percent CI: 0.7, 2.1) and HR = 1.5 (95 percent CI: 1.0, 2.5) for BMIs of 23.0–24.9 and ≥25.0, respectively, vs. BMI < 23.0). However, this effect of obesity was much weaker among premenopausal women (HR = 1.0 (95 percent CI: 0.6, 1.5) and HR = 1.2 (95 percent CI: 0.8, 1.8) for the above BMI categories).

We also conducted analyses stratified on TNM stage and ER/PR status. Eighty-two percent of study subjects had early-stage breast cancer (TNM stage 0–II). Among those women, increased BMI was inversely related to survival, although the 95 percent confidence interval for the hazard ratio included the null value. The small number of patients with both late-stage breast cancer and a high BMI prohibited detailed analysis of this subgroup. The associations of BMI and waist:hip ratio with breast cancer survival did not differ across strata of ER/PR status (data not shown).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
In this population-based cohort study of 1,455 patients with primary breast cancer, we found that being overweight (BMI ≥ 25.0) at or soon after cancer diagnosis was inversely related to both overall survival and disease-free survival. This association persisted after adjustment for known breast cancer prognostic factors, including age at diagnosis, education, TNM stage, ER/PR status, chemotherapy, radiotherapy, and tamoxifen treatment. We found no association between waist:hip ratio and breast cancer survival.

In Caucasian populations, obesity at the time of breast cancer diagnosis has been reported to be associated with poorer survival and an increased likelihood of recurrence, though not all studies investigating this relation have found such an association (2Go–5Go, 7Go–12Go, 14Go–22Go, 24Go–27Go). It is known that the body composition profile of Asian populations differs from that of Caucasian and African-American populations. To our knowledge, only two epidemiologic studies have examined the relation between breast cancer survival and obesity in Asian populations (6Go, 31Go). Both involved hospital-based patient cohorts with small sample sizes. Among 593 breast cancer cases, Kimura (31Go) found no significant difference in the 5-year survival rate, but a significant decrease in the 10-year survival rate was detected between the obese group and the lean group, especially among postmenopausal women. After follow-up of 213 breast cancer patients, Kyogoku et al. (6Go) reported that BMI measured 1–3 months after surgery was positively related to increased risk of mortality (ptrend < 0.01) after adjustment for other prognostic factors and potential confounders. Our results are consistent with those of some previous studies conducted in Caucasian or Asian populations (5Go–9Go, 12Go, 15Go–19Go, 21Go, 20Go, 27Go), but they disagree with the results of other studies (4Go, 10Go, 11Go, 13Go, 14Go, 20Go, 25Go, 26Go, 28Go, 30Go).

Several mechanisms could account for these observations. Obesity has been found to be associated with a more advanced tumor stage and/or greater lymph node involvement at diagnosis (33Go); the obesity-survival association might reflect the effect of advanced stage at cancer diagnosis. BMI was related to stage of disease at diagnosis in our study population. However, our study and other studies in which the majority of subjects were early-stage breast cancer patients found a positive association between BMI and survival (24Go, 34Go). Further analysis stratified by disease stage in our study showed that being overweight was adversely related to survival among patients with early-stage breast cancer. These results suggest that late stage at cancer diagnosis among overweight women may not be the sole explanation for the observed association between weight and survival.

Another possible explanation is the high concentrations of estrone, estradiol, and testosterone in overweight and obese breast cancer patients stemming from the conversion of androstenedione in adipose tissue. Obesity has also been shown to be related to lower levels of sex hormone-binding globulin, resulting in higher levels of free estradiol and free testosterone (35Go, 36Go). Therefore, estrogen-sensitive tissues in overweight/obese women are subject to higher estrogen stimulation, which may lead to more rapid growth of malignant cells or may promote metastases. Since adipose tissue is the primary source of circulating estrogen in postmenopausal women, estrogen production is directly correlated with body weight after menopause. Thus, it is possible that overweight/obesity may have a stronger effect on survival among postmenopausal patients. Although the 95 percent confidence interval for the hazard ratio included the null value, analyses stratified by menopausal status in our study supported this hypothesis, which is consistent with some previous studies (18Go, 21Go). In addition, adipose tissue produces a group of growth factors, cytokines, and adipocytokines (including leptin, tumor necrosis factor-{alpha}, interleukin-6, heparin-binding epidermal growth factor, vascular endothelial growth factor, and hepatocyte growth factor), most of which can stimulate angiogenesis and promote tumor growth and metastasis (37Go). A number of adipocytokines also play important roles in the modulation of insulin, which has been found to correlate with breast cancer prognosis (37Go, 38Go).

Higher waist:hip ratio, a marker of hyperinsulinemia, represents greater abdominal fat distribution. Results from previous studies on waist:hip ratio and breast cancer prognosis have been limited and inconsistent (13Go, 23Go, 29Go, 39Go). We failed to find an independent association between body fat distribution and breast cancer survival among either premenopausal women or postmenopausal women in our population.

Strengths of our study include the population-based patient cohort, the high response and follow-up rates, the professional measurement of anthropometric factors, and the detailed information on cancer characteristics and treatments. Additionally, the median length of follow-up was 5.1 years (25th–75th percentiles, 4.6–5.6), which provided relatively good statistical power. However, there are a few limitations that should be considered when evaluating our results. The majority of women in this study received adjuvant chemotherapy as part of their regular treatment for breast cancer. However, specific information on chemotherapy and the duration of chemotherapy was not available for all patients in this study, which limited our ability to examine the effect of potential interaction between overweight and chemotherapy on disease prognosis. On the basis of our ongoing study of breast cancer survival in Shanghai, we found that 95.4 percent of breast cancer patients completed their chemotherapy within 6 months after cancer diagnosis, and the duration of treatment was not related to BMI at cancer diagnosis. In several studies, excessive weight and weight gain after diagnosis of breast cancer have been suggested to reduce overall and/or disease-free survival and to increase rates of recurrence and relapse (40Go–42Go). However, information on weight changes after cancer treatment was not available for our study subjects, which limited our ability to evaluate the association between weight changes after diagnosis and breast cancer survival. The self-reported information on disease relapse and cause of death may have been subject to misclassification bias. Such misclassification is likely to have been nondifferential and to have biased the results towards the null. As we noted above, information regarding ER/PR status was abstracted from hospital records and was missing for approximately 30 percent of study subjects, which compromised our ability to evaluate associations of obesity with breast cancer survival by ER/PR status. Lastly, the lack of information on tamoxifen use for a sizable number of subjects, particularly those who died before the follow-up survey, hampered our ability to evaluate the joint effect of obesity and tamoxifen use on breast cancer survival.

In summary, we found that being overweight at or soon after diagnosis of breast cancer was related to lower rates of overall survival and disease-free survival. Our results, in conjunction with those of other studies, support the idea that interventions directed at weight control may have a substantial effect not only on breast cancer incidence but also on breast cancer survival.


   ACKNOWLEDGMENTS
 
This study was funded by US Public Health Service grant R01CA64277 from the National Cancer Institute.

The authors are grateful to the research staff of the Shanghai Breast Cancer Study. The authors thank Bethanie Hull for technical support.

Conflict of interest: none declared.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

  1. Feigelson HS, Jonas CR, Teras LR, et al. Weight gain, body mass index, hormone replacement therapy, and postmenopausal breast cancer in a large prospective study. Cancer Epidemiol Biomarkers Prev 2004;13:220–4.[Abstract/Free Full Text]
  2. Abe R, Kumagai N, Kimura M, et al. Biological characteristics of breast cancer in obesity. Tohoku J Exp Med 1976;120:351–9.[Web of Science][Medline]
  3. Tartter PI, Papatestas AE, Ioannovich J, et al. Cholesterol and obesity as prognostic factors in breast cancer. Cancer 1981;47:2222–7.[CrossRef][Web of Science][Medline]
  4. Greenberg ER, Vessey MP, McPherson K, et al. Body size and survival in premenopausal breast cancer. Br J Cancer 1985;51:691–7.[Web of Science][Medline]
  5. Hebert JR, Augustine A, Barone J, et al. Weight, height and body mass index in the prognosis of breast cancer: early results of a prospective study. Int J Cancer 1988;42:315–18.[Web of Science][Medline]
  6. Kyogoku S, Hirohata T, Takeshita S, et al. Survival of breast-cancer patients and body size indicators. Int J Cancer 1990;46:824–31.[Web of Science][Medline]
  7. Vatten LJ, Foss OP, Kvinnsland S. Overall survival of breast cancer patients in relation to preclinically determined total serum cholesterol, body mass index, height and cigarette smoking: a population-based study. Eur J Cancer 1991;27:641–6.[Web of Science][Medline]
  8. Senie RT, Rosen PP, Rhodes P, et al. Obesity at diagnosis of breast carcinoma influences duration of disease-free survival. Ann Intern Med 1992;16:26–32.
  9. Tornberg S, Carstensen J. Serum beta-lipoprotein, serum cholesterol and Quetelet's index as predictors for survival of breast cancer patients. Eur J Cancer 1993;29A:2025–30.[CrossRef]
  10. Katoh A, Watzlaf VJ, D'Amico F. An examination of obesity and breast cancer survival in post-menopausal women. Br J Cancer 1994;70:928–33.[Web of Science][Medline]
  11. Jain M, Miller AB. Pre-morbid body size and the prognosis of women with breast cancer. Int J Cancer 1994;59:363–8.[Web of Science][Medline]
  12. Bastarrachea J, Hortobagyi GN, Smith TL, et al. Obesity as an adverse prognostic factor for patients receiving adjuvant chemotherapy for breast cancer. Ann Intern Med 1994;120:18–25.[Abstract/Free Full Text]
  13. den Tonkelaar I, de Waard F, Seidell JC, et al. Obesity and subcutaneous fat patterning in relation to survival of postmenopausal breast cancer patients participating in the DOM-project. Breast Cancer Res Treat 1995;34:129–37.[CrossRef][Web of Science][Medline]
  14. Obermair A, Kurz C, Hanzal E, et al. The influence of obesity on the disease-free survival in primary breast cancer. Anticancer Res 1995;15:2265–9.[Web of Science][Medline]
  15. Zhang S, Folsom AR, Sellers TA, et al. Better breast cancer survival for postmenopausal women who are less overweight and eat less fat. The Iowa Women's Health Study. Cancer 1995;76:275–83.[CrossRef][Web of Science][Medline]
  16. Maehle BO, Tretli S. Pre-morbid body-mass-index in breast cancer: reversed effect on survival in hormone receptor negative patients. Breast Cancer Res Treat 1996;41:123–30.[CrossRef][Web of Science][Medline]
  17. Newman SC, Lees AW, Jenkins H. The effect of body mass index and oestrogen receptor level on survival of breast cancer patients. Int J Epidemiol 1997;26:484–90.[Abstract/Free Full Text]
  18. Chang S, Alderfer JR, Asmar L, et al. Inflammatory breast cancer survival: the role of obesity and menopausal status at diagnosis. Breast Cancer Res Treat 2000;64:157–63.[CrossRef][Web of Science][Medline]
  19. Daling JR, Malone KE, Doody DR, et al. Relation of body mass index to tumor markers and survival among young women with invasive ductal breast carcinoma. Cancer 2001;92:720–9.[CrossRef][Web of Science][Medline]
  20. Marret H, Rerrotin F, Bougnoux P, et al. Low body mass index is an independent predictive factor of local recurrence after conservative treatment for breast cancer. Breast Cancer Res Treat 2001;66:17–23.[CrossRef][Web of Science][Medline]
  21. Petrelli JM, Calle EE, Rodriguez C, et al. Body mass index, height, and postmenopausal breast cancer mortality in a prospective cohort of US women. Cancer Causes Control 2002;13:325–32.[CrossRef][Web of Science][Medline]
  22. Dignam JJ, Wieand K, Johnson KA, et al. Obesity, tamoxifen use, and outcomes in women with estrogen receptor-positive early-stage breast cancer. J Natl Cancer Inst 2003;95:1467–76.[Abstract/Free Full Text]
  23. Borugian MJ, Sheps SB, Kim-Sing C, et al. Waist-to-hip ratio and breast cancer mortality. Am J Epidemiol 2003;158:963–8.[Abstract/Free Full Text]
  24. Enger SM, Greif JM, Polikoff J, et al. Body weight correlates with mortality in early-stage breast cancer. Arch Surg 2004;139:954–60.[Abstract/Free Full Text]
  25. Carmichael AR, Bendall S, Lockerbie L, et al. Does obesity compromise survival in women with breast cancer? Breast 2004;13:93–6.[CrossRef][Web of Science][Medline]
  26. Menon KV, Hodge A, Houghton J, et al. Body mass index, height and cumulative menstrual cycles at the time of diagnosis are not risk factors for poor outcome in breast cancer. Breast 1999;8:328–33.[CrossRef][Web of Science][Medline]
  27. Berclaz G, Li S, Price KN, et al. Body mass index as a prognostic feature in operable breast cancer: the International Breast Cancer Study Group experience. Ann Oncol 2004;15:875–84.[Abstract/Free Full Text]
  28. Rock CL, Demark-Wahnefried W. Nutrition and survival after the diagnosis of breast cancer: a review of the evidence. J Clin Oncol 2002;20:3302–16.[Abstract/Free Full Text]
  29. Kumar NB, Cantor A, Allen K, et al. Android obesity at diagnosis and breast carcinoma survival: evaluation of the effects of anthropometric variables at diagnosis, including body composition and body fat distribution and weight gain during life span, and survival from breast carcinoma. Cancer 2000;88:2751–7.[CrossRef][Web of Science][Medline]
  30. Clegg LX, Li FP, Hankey BF, et al. Cancer survival among US whites and minorities. Arch Intern Med 2002;162:1985–93.[Abstract/Free Full Text]
  31. Kimura M. Obesity as prognostic factors in breast cancer. Diabetes Res Clin Pract 1990;10(suppl 1):S247–51.
  32. Gallagher D. Overweight and obesity BMI cut-offs and their relation to metabolic disorders in Koreans/Asians. Obes Res 2004;12:440–1.[Web of Science][Medline]
  33. Moorman PG, Jones BA, Millikan RC, et al. Race, anthropometric factors, and stage at diagnosis of breast cancer. Am J Epidemiol 2001;153:284–91.[Abstract/Free Full Text]
  34. Tretli S, Haldorsen T, Ottestad L. The effect of pre-morbid height and weight on the survival of breast cancer patients. Br J Cancer 1990;62:299–303.[Web of Science][Medline]
  35. Schapira DV, Kumar NB, Lyman GH. Obesity, body fat distribution, and sex hormones in breast cancer patients. Cancer 1991;67:2215–18.[CrossRef][Web of Science][Medline]
  36. MeTiernan A, Rajan KB, Tworoger SS, et al. Adiposity and sex hormones in postmenopausal breast cancer survivors. J Clin Oncol 2003;21:1961–6.[Abstract/Free Full Text]
  37. Rose DP, Komninou D, Stephenson GD. Obesity, adipocytokines, and insulin resistance in breast cancer. Obes Rev 2004;5:153–65.[CrossRef][Medline]
  38. Goodwin PJ, Ennis M, Pritchard KI, et al. Fasting insulin and outcome in early-stage breast cancer: results of a prospective cohort study. J Clin Oncol 2002;20:42–51.[Abstract/Free Full Text]
  39. Folsom AR, Kushi LH, Anderson KE, et al. Association of general and abdominal obesity with multiple health outcomes in older women. Arch Intern Med 2000;160:2117–28.[Abstract/Free Full Text]
  40. 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 1986;7:23–30.[CrossRef][Web of Science][Medline]
  41. Goodwin PJ, Panzarella T, Boyd NF. Weight gain in women with localized breast cancer—a descriptive study. Breast Cancer Res Treat 1988;11:59–66.[CrossRef][Web of Science][Medline]
  42. Camoriano JK, Loprinzi CL, Ingle JN, et al. Weight change in women with adjuvant therapy or observed following mastectomy for node-positive breast cancer. J Clin Oncol 1990;8:1327–34.[Abstract]

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