Obesity and breast cancer prognosis: Evidence, challenges, and opportunities

Journal of Clinical Oncology

Volumn 34, Issue 35, 2016, Pages 4203-4216

  Jiralerspong, Sao ^a   Goodwin, Pamela J ^b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN RECEPTOR;

BODY MASS; BODY SIZE; BREAST CANCER; CANCER CHEMOTHERAPY; CANCER GROWTH; CANCER HORMONE THERAPY; CANCER MORTALITY; CANCER PATIENT; CANCER PROGNOSIS; CANCER RECURRENCE; CANCER RISK; CANCER STAGING; CANCER SURGERY; CANCER SURVIVAL; CANCER THERAPY; DIET THERAPY; DISEASE ASSOCIATION; FEMALE; HUMAN; LIFESTYLE MODIFICATION; MULTIMODALITY CANCER THERAPY; OBESITY; OUTCOME ASSESSMENT; PATIENT COUNSELING; PHYSICAL ACTIVITY; PHYSICAL INACTIVITY; POSTMENOPAUSE; PRIORITY JOURNAL; REVIEW; WEIGHT REDUCTION; BREAST NEOPLASMS; COMPLICATION; MORTALITY; PATHOLOGY; PROGNOSIS; RISK FACTOR; SURVIVAL ANALYSIS; TUMOR RECURRENCE;

BREAST NEOPLASMS; FEMALE; HUMANS; NEOPLASM RECURRENCE, LOCAL; OBESITY; PROGNOSIS; RISK FACTORS; SURVIVAL ANALYSIS;

EID: 85002968967     PISSN: 0732183X     EISSN: 15277755     Source Type: Journal    
DOI: 10.1200/JCO.2016.68.4480     Document Type: Review

References (99)

1. Flegal KM, Carroll MD, Ogden CL, et al: Prevalence and trends in obesity among US adults, 1999-2008. JAMA 303:235-241, 2010
2. Ogden CL, Carroll MD, Kit BK, et al: sPrevalence of childhood and adult obesity in the United States, 2011-2012. JAMA 311:806-814, 2014
3. Ng M, Fleming T, RobinsonM, et al: Global, regional, and national prevalence of overweight and obesity in children and adults during 1980-2013: A systematic analysis for the Global Burden of Disease Study 2013. Lancet 384:766-781, 2014
4. Goodwin PJ, Stambolic V: Impact of the obesity epidemic on cancer. Annu Rev Med 66:281-296, 2015
5. Chlebowski RT, Aiello E, McTiernan A: Weight loss in breast cancer patient management. J Clin Oncol 20:1128-1143, 2002
6. Parekh N, Chandran U, Bandera EV: Obesity in cancer survival. Annu Rev Nutr 32:311-342, 2012
7. Suzuki R, Orsini N, Saji S, et al: Body weight and incidence of breast cancer defined by estrogen and progesterone receptor status: A meta-analysis. Int J Cancer 124:698-712, 2009
8. Pierobon M, Frankenfeld CL: Obesity as a risk factor for triple-negative breast cancers: A systematic review and meta-analysis. Breast Cancer Res Treat 137:307-314, 2013
9. Wu Y, Zhang D, Kang S: Physical activity and risk of breast cancer: A meta-analysis of prospective studies. Breast Cancer Res Treat 137:869-882, 2013
10. Protani M, Coory M, Martin JH: Effect of obesity on survival of women with breast cancer: Systematic review and meta-analysis. Breast Cancer Res Treat 123:627-635, 2010
11. Niraula S, Ocana A, Ennis M, et al: Body size and breast cancer prognosis in relation to hormone receptor and menopausal status: A meta-analysis. Breast Cancer Res Treat 134:769-781, 2012
12. Chan DS, Vieira AR, Aune D, et al: Bodymass index and survival in women with breast cancer: Systematic literature review and meta-analysis of 82 follow-up studies. Ann Oncol 25:1901-1914, 2014
13. Majed B, Moreau T, Senouci K, et al: Is obesity an independent prognosis factor in woman breast cancer? Breast Cancer Res Treat 111:329-342, 2008
14. Chen X, Lu W, Zheng W, et al: Obesity and weight change in relation to breast cancer survival. Breast Cancer Res Treat 122:823-833, 2010
15. Ewertz M, Jensen MB, Gunnarsdóttir KA, et al: Effect of obesity on prognosis after early-stage breast cancer. J Clin Oncol 29:25-31, 2011
16. Goodwin PJ, Ennis M, Pritchard KI, et al: Insulin- and obesity-related variables in early-stage breast cancer: Correlations and time course of prognostic associations. J Clin Oncol 30:164-171, 2012
17. Nechuta S, Chen WY, Cai H, et al: A pooled analysis of post-diagnosis lifestyle factors in association with late estrogen-receptor-positive breast cancer prognosis. Int J Cancer 138:2088-2097, 2016
18. Sestak I, Distler W, Forbes JF, et al: Effect of body mass index on recurrences in tamoxifen and anastrozole treated women: An exploratory analysis from the ATAC trial. J Clin Oncol 28:3411-3415, 2010
19. Ewertz M, Gray KP, Regan MM, et al: Obesity and risk of recurrence or death after adjuvant endocrine therapywith letrozole or tamoxifen in the Breast International Group 1-98 trial. J Clin Oncol 30:3967-3975, 2012
20. Playdon MC, Bracken MB, Sanft TB, et al: Weight gain after breast cancer diagnosis and all-cause mortality: Systematic review and meta-analysis. J Natl Cancer Inst 107: djv275, 2015
21. Ligibel JA, Cirrincione CT, Liu M, et al: Body mass index, PAM50 subtype, and outcomes in nodepositive breast cancer: CALGB 9741 (Alliance). J Natl Cancer Inst 25:107, 2015
22. Pajares B, Pollán M, Martín M, et al: Obesity and survival in operable breast cancer patients treated with adjuvant anthracyclines and taxanes according to pathological subtypes: A pooled analysis. Breast Cancer Res 15:R105, 2013
23. Fontanella C, Lederer B, Gade S, et al: Impact of body mass index on neoadjuvant treatment outcome: A pooled analysis of eight prospective neoadjuvant breast cancer trials. Breast Cancer Res Treat 150:127-139, 2015
24. Widschwendter P, Friedl TW, Schwentner L, et al: The influence of obesity on survival in early, high-risk breast cancer: Results from the randomized SUCCESS A trial. Breast Cancer Res 17:129, 2015
25. Hao S, Liu Y, Yu KD, et al: Overweight as a prognostic factor for triple-negative breast cancers in Chinese women. PLoS One 10:e0129741, 2015
26. Bonsang-Kitzis H, Chaltier L, Belin L, et al: Beyond axillary lymph node metastasis, BMI and menopausal status are prognostic determinants for triple-negative breast cancer treated by neoadjuvant chemotherapy. PLoSOne 10:e0144359, 2015
27. [Erratum: PLoS One 11:e0159123, 2016]
28. Pan H, Gray RG: Effect of obesity on prognosis in premenopausal ER+ early breast cancer: EBCTCG data on 80, 000 patients in 70 trials. J Clin Oncol 32:5s, 2014 (suppl; abstr 503)
29. Sparano JA, WangM, Zhao F, et al: Obesity at diagnosis is associated with inferior outcomes in hormone receptor-positive operable breast cancer. Cancer 118:5937-5946, 2012
30. Sparano JA, Zhao F, Martino S, et al: Longterm follow-up of the E1199 phase III trial evaluating the role of taxane and schedule in operable breast cancer. J Clin Oncol 33:2353-2360, 2015
31. Cecchini RS, Swain SM, Costantino JP, et al: Body mass index at diagnosis and breast cancer survival prognosis in clinical trial populations from NRG Oncology/NSABP B-30, B-31, B-34, and B-38. Cancer Epidemiol Biomarkers Prev 25:51-59, 2016
32. Dignam JJ, Wieand K, Johnson KA, et al: Effects of obesity and race on prognosis in lymph nodenegative, estrogen receptor-negative breast cancer. Breast Cancer Res Treat 97:245-254, 2006
33. Jiralerspong S, Kim ES, Dong W, et al: Obesity, diabetes, and survival outcomes in a large cohort of early-stage breast cancer patients. Ann Oncol 24:2506-2514, 2013
34. Dawood S, Lei X, Litton JK, et al: Impact of body mass index on survival outcome amongwomen with early stage triple-negative breast cancer. Clin Breast Cancer 12:364-372, 2012
35. Tait S, Pacheco JM, Gao F, et al: Body mass index, diabetes, and triple-negative breast cancer prognosis. Breast Cancer Res Treat 146:189-197, 2014
36. Ademuyiwa FO, Groman A, O'Connor T, et al: Impact of body mass index on clinical outcomes in triple-negative breast cancer. Cancer 117:4132-4140, 2011
37. Mowad R, Chu QD, Li BD, et al: Does obesity have an effect on outcomes in triple-negative breast cancer? J Surg Res 184:253-259, 2013
38. Dunlap SM, Chiao LJ, Nogueira L, et al: Dietary energy balance modulates epithelial-tomesenchymal transition and tumor progression in murine claudin-low and basal-like mammary tumor models. Cancer Prev Res (Phila) 5:930-942, 2012
39. Ford NA, Rossi EL, Barnett K, et al: Omega-3-acid ethyl esters block the protumorigenic effects of obesity in mouse models of postmenopausal basallike and claudin-low breast cancer. Cancer Prev Res (Phila) 8:796-806, 2015
40. Sundaram S, Freemerman AJ, Johnson AR, et al: Role of HGF in obesity-associated tumorigenesis: C3 (1)-TAg mice as a model for human basal-like breast cancer. Breast Cancer Res Treat 142:489-503, 2013
41. Chlebowski RT, Blackburn GL, Thomson CA, et al: Dietary fat reduction and breast cancer outcome: Interim efficacy results from the Women's Intervention Nutrition Study. J Natl Cancer Inst 98:1767-1776, 2006
42. Chlebowski RT, Blackburn GL: Final survival analysis from the randomized Women's Intervention Nutrition Study (WINS) evaluating dietary invention as adjuvant breast cancer therapy. Presented at San Antonio Breast Cancer Symposium, San Antonio, TX, December 9-13 2014
43. Mazzarella L, Disalvatore D, Bagnardi V, et al: Obesity increases the incidence of distant metastases in oestrogen receptor-negative human epidermal growth factor receptor 2-positive breast cancer patients. Eur J Cancer 49:3588-3597, 2013
44. Crozier JA, Moreno-Aspitia A, Ballman KV, et al: Effect of body mass index on tumor characteristics and disease-free survival in patients from the HER2-positive adjuvant trastuzumab trial N9831. Cancer 119:2447-2454, 2013
45. 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 95:1467-1476, 2003
46. Gnant M, Pfeiler G, Stöger H, et al: The predictive impact of body mass index on the efficacy of extended adjuvant endocrine treatment with anastrozole in postmenopausal patients with breast cancer: An analysis of the randomised ABCSG-6a trial. Br J Cancer 109:589-596, 2013
47. Pfeiler G, Kö nigsberg R, Fesl C, et al: Impact of body mass index on the efficacy of endocrine therapy in premenopausal patients with breast cancer: An analysis of the prospective ABCSG-12 trial. J Clin Oncol 29:2653-2659, 2011
48. Pagani O, Regan MM, Walley BA, et al: Adjuvant exemestane with ovarian suppression in premenopausal breast cancer. N Engl J Med 371:107-118, 2014
49. Francis PA, Regan MM, Fleming GF, et al: Adjuvant ovarian suppression in premenopausal breast cancer. N Engl J Med 372:436-446, 2015
50. Bellet M, Gray KP, Francis PA, et al: Twelvemonth estrogen levels in premenopausal women with hormone receptor-positive breast cancer receiving adjuvant triptorelin plus exemestane or tamoxifen in the Suppression of Ovarian Function Trial (SOFT): The SOFT-EST substudy. J Clin Oncol 34:1584-1593, 2016
51. O'Shaughnessy J, Yardley DA, Burris HA, et al: Randomized phase 3 trial of adjuvant letrozole vs anastrozole in postmenopausal patientswith hormone receptor-positive, node-positive early breast cancer: Final efficacy and safety results of the Femara vs Anastrozole Clinical Evaluation (FACE) trial. Presented at San Antonio Breast Cancer Symposium, San Antonio, TX, December 8-12, 2015
52. Ioannides SJ, Barlow PL, Elwood JM, et al: Effect of obesity on aromatase inhibitor efficacy in postmenopausal, hormone receptor-positive breast cancer: A systematic review. Breast Cancer Res Treat 147:237-248, 2014
53. Bhatnagar AS: The discovery and mechanism of action of letrozole. Breast Cancer Res Treat 105:7-17, 2007 (suppl 1)
54. Lønning PE: The potency and clinical efficacy of aromatase inhibitors across the breast cancer continuum. Ann Oncol 22:503-514, 2011
55. Folkerd EJ, Dixon JM, Renshaw L, et al: Suppression of plasma estrogen levels by letrozole and anastrozole is related to body mass index in patients with breast cancer. J Clin Oncol 30:2977-2980, 2012
56. Pfeiler G, Königsberg R, Hadji P, et al: Impact of body mass index on estradiol depletion by aromatase inhibitors in postmenopausal women with early breast cancer. Br J Cancer 109:1522-1527, 2013
57. Decker DA, Reynolds RB, Molthrop DC, et al: Obesity and nonadherence correlate with elevated serum estradiol levels in postmenopausal women receiving adjuvant aromatase inhibitor therapy. Breast J 20:553-554, 2014
58. Kyvernitakis I, Knö ll D, Struck M, et al: Impact of BMI on serum estradiol and bone turnover markers in postmenopausal women with hormone-sensitive early breast cancer treated with anastrozole. J Cancer Res Clin Oncol 140:159-166, 2014
59. Diorio C, Lemieux J, Provencher L, et al: Aromatase inhibitors in obese breast cancer patients are not associated with increased plasma estradiol levels. Breast Cancer Res Treat 136:573-579, 2012
60. Iyengar NM, Hudis CA, Dannenberg AJ: Obesity and cancer: Llocal and systemic mechanisms. Annu Rev Med 66:297-309, 2015
61. Allott EH, Hursting SD: Obesity and cancer: Mechanistic insights from transdisciplinary studies. Endocr Relat Cancer 22:R365-R386, 2015
62. Park J, Morley TS, Kim M, et al: Obesity and cancer-mechanisms underlying tumour progression and recurrence. Nat Rev Endocrinol 10:455-465, 2014
63. 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 20:42-51, 2002
64. Goodwin PJ: Obesity and breast cancer outcomes: How much evidence is needed to change practice? J Clin Oncol 34:646-648, 2016
65. Pierce JP, Natarajan L, Caan BJ, et al: Influence of a diet very high in vegetables, fruit, and fiber and low in fat on prognosis following treatment for breast cancer: The Women's Healthy Eating and Living (WHEL) randomized trial. JAMA 298:289-298, 2007
66. Pierce JP: Diet and breast cancer prognosis: Making sense of the Women's Healthy Eating and Living and Women's Intervention Nutrition Study trials. Curr Opin Obstet Gynecol 21:86-91, 2009
67. Chlebowski R, Aragaki AK, Anderson GL, et al: Low-fat dietary pattern and breast cancer mortality in the Women's Health Initiative (WHI) randomized trial. Presented at American Association for Cancer Research Annual Meeting, New Orleans, LA, April 16-20, 2016
68. Playdon M, Thomas G, Sanft T, et al: Weight loss intervention for breast cancer survivors: A systematic review. Curr Breast Cancer Rep 5:222-246, 2013
69. Reeves MM, Terranova CO, Eakin EG, et al: Weight loss intervention trials in women with breast cancer: A systematic review. Obes Rev 15:749-768, 2014
70. Goodwin PJ, Segal RJ, Vallis M, et al: Randomized trial of a telephone-based weight loss intervention in postmenopausal women with breast cancer receiving letrozole: The LISA trial. J Clin Oncol 32:2231-2239, 2014
71. Rock CL, Flatt SW, Byers TE, et al: Results of the Exercise and Nutrition to Enhance Recovery and Good Health for You (ENERGY) Trial: A behavioral weight loss intervention in overweight or obese breast cancer survivors. J Clin Oncol 33:3169-3176, 2015
72. Harrigan M, Cartmel B, Loftfield E, et al: Randomized trial comparing telephone versus inperson weight loss counseling on body composition and circulating biomarkers in women treated for breast cancer: The Lifestyle, Exercise, and Nutrition (LEAN) study. J Clin Oncol 34:669-676, 2016
73. Villarini A, Pasanisi P, Traina A, et al: Lifestyle and breast cancer recurrences: The DIANA-5 trial. Tumori 98:1-18, 2012
74. Rack B, Andergassen U, Neugebauer J, et al: The German SUCCESS C study: The first European lifestyle study on breast cancer. Breast Care (Basel) 5:395-400, 2010
75. Sacks FM, Bray GA, Carey VJ, et al: Comparison of weight-loss diets with different compositions of fat, protein, and carbohydrates. N Engl J Med 360:859-873, 2009
76. Hu T, Mills KT, Yao L, et al: Effects of lowcarbohydrate diets versus low-fat diets on metabolic risk factors: A meta-analysis of randomized controlled clinical trials. Am J Epidemiol 176:S44-S54, 2012 (suppl 7)
77. Johnston BC, Kanters S, Bandayrel K, et al: Comparison of weight loss among named diet programs in overweight and obese adults: A metaanalysis. JAMA 312:923-933, 2014
78. Shai I, Schwarzfuchs D, Henkin Y, et al: Weight loss with a low-carbohydrate, Mediterranean, or low-fat diet. N Engl J Med 359:229-241, 2008
79. Dowling RJ, Niraula S, Stambolic V, et al: Metformin in cancer: Translational challenges. J Mol Endocrinol 48:R31-R43, 2012
80. Jiralerspong S, Palla SL, Giordano SH, et al: Metformin and pathologic complete responses to neoadjuvant chemotherapy in diabetic patients with breast cancer. J Clin Oncol 27:3297-3302, 2009
81. Goodwin PJ, Ligibel JA, Stambolic V: Metformin in breast cancer: Time for action. J Clin Oncol 27:3271-3273, 2009
82. Camacho L, Dasgupta A, Jiralerspong S: Metformin in breast cancer: An evolving mystery. Breast Cancer Res 17:88, 2015
83. Pizzuti L, Vici P, Di Lauro L, et al: Metformin and breast cancer: Basic knowledge in clinical context. Cancer Treat Rev 41:441-447, 2015
84. Lord SR, Patel N, Liu D, et al: Neoadjuvant window studies of metformin and biomarker development for drugs targeting cancermetabolism. J Natl Cancer Inst Monogr 2015:81-86, 2015
85. Goodwin PJ, Parulekar WR, Gelmon KA, et al: Effect of metformin vs placebo on and metabolic factors in NCIC CTG MA.32. J Natl Cancer Inst 4:107, 2015
86. Pi-Sunyer X, Astrup A, Fujioka K, et al: A randomized, controlled trial of 3.0 mg of liraglutide in weight management. N Engl J Med 373:11-22, 2015
87. Pi-Sunyer X; SCALE Obesity and Prediabetes Investigators: Liraglutide in weight management. N Engl J Med 373:1781-1782, 2015
88. Fischer JP, Tuggle CT, Au A, et al: A 30-day risk assessment of mastectomy alone compared to immediate breast reconstruction (IBR). J Plast Surg Hand Surg 48:209-215, 2014
89. Jeevan R, Browne JP, Pereira J, et al: Socioeconomic deprivation and inpatient complication rates following mastectomy and breast reconstruction surgery. Br J Surg 102:1064-1070, 2015
90. Fischer JP, Nelson JA, Kovach SJ, et al: Impact of obesity on outcomes in breast reconstruction: Analysis of 15, 937 patients from the ACS-NSQIP datasets. J Am Coll Surg 217:656-664, 2013
91. Fischer JP, Cleveland EC, Nelson JA, et al: Breast reconstruction in the morbidly obese patient: Assessment of 30-day complications using the 2005 to 2010 National Surgical Quality Improvement Program data sets. Plast Reconstr Surg 132:750-761, 2013
92. Fischer JP, Wes AM, Tuggle CT, et al: Venous thromboembolism risk in mastectomy and immediate breast reconstruction: Analysis of the 2005 to 2011 American College of Surgeons National Surgical Quality Improvement Program data sets. Plast Reconstr Surg 133:263e-273e, 2014
93. DiSipio T, Rye S, Newman B, et al: Incidence of unilateral arm lymphoedema after breast cancer: A systematic review and meta-analysis. Lancet Oncol 14:500-515, 2013
94. Griggs JJ, Mangu PB, Anderson H, et al: Appropriate chemotherapy dosing for obese adult patients with cancer: American Society of Clinical Oncology clinical practice guideline. J Clin Oncol 30:1553-1561, 2012
95. Lyman GH, Sparreboom A: Chemotherapy dosing in overweight and obese patientswith cancer. Nat Rev Clin Oncol 10:451-459, 2013
96. Mantarro S, Rossi M, Bonifazi M, et al: Risk of severe cardiotoxicity following treatment with trastuzumab: A meta-analysis of randomized and cohort studies of 29, 000 women with breast cancer. Intern Emerg Med 11:123-140, 2016
97. Rock CL, Doyle C, Demark-Wahnefried W, et al: Nutrition and physical activity guidelines for cancer survivors. CA Cancer J Clin 62:243-274, 2012
98. Runowicz CD, Leach CR, Henry NL, et al: American Cancer Society/American Society of Clinical Oncology breast cancer survivorship care guideline. J Clin Oncol 34:611-635, 2016
99. Zhong S, Jiang T, Ma T, et al: Association between physical activity and mortality in breast cancer: A meta-analysis of cohort studies. Eur J Epidemiol 29:391-404, 2014