https://doi.org/10.1038/s41523-021-00241-9 ·
Видання: npj Breast Cancer, 2021, №1
Видавець: Springer Science and Business Media LLC
Автори:
- Natansh D. Modi
- Jin Quan Eugene Tan
- Andrew Rowland
- Bogda Koczwara
- Ahmad Y. Abuhelwa
- Ganessan Kichenadasse
- Ross A. McKinnon
- Michael D. Wiese
- Michael J. Sorich
- Ashley M. Hopkins
Анотація
AbstractWhile many studies have evaluated the relationship between BMI and breast cancer outcomes, it is unclear whether this relationship is consistent between early breast cancer (BC) and advanced BC. The study included 5099 patients with HER2 positive early BC (EBC) and 3496 with HER2 positive advanced BC (ABC). In the EBC cohort, higher BMI was associated with worse overall survival (OS) (HR [95% CI]: overweight = 1.30 [1.13–1.51]; obese = 1.37 [1.14–1.64], P = < 0.001), and worse disease-free survival (overweight = 1.10 [0.98–1.24]; obese = 1.20 [1.04–1.39], P = 0.061). In contrast, for the ABC cohort, higher BMI was significantly associated with improved OS (overweight = 0.85 [0.76–0.96]; obese = 0.82 [0.72–0.95], P = 0.014), and progression-free survival (overweight = 0.91 [0.83–1.01]; obese = 0.87 [0.77–0.98], P = 0.034). In this large high-quality dataset, higher BMI was independently associated with worse survival in EBC, paradoxically in ABC higher BMI was independently associated with improved survival.
Джерела фінансування
- Cancer Council South Australia
- National Breast Cancer Foundation
Список літератури
- Ellingjord-Dale, M. et al. Number of risky lifestyle behaviors and breast cancer risk. JNCI Cancer Spectr. 2, 8 (2018).
https://doi.org/10.1093/jncics/pky030 - Liu, K. et al. Association between body mass index and breast cancer risk: evidence based on a dose-response meta-analysis. Cancer Manag. Res. 10, 143–151 (2018).
https://doi.org/10.2147/CMAR.S144619 - Key, T. J. et al. Steroid hormone measurements from different types of assays in relation to body mass index and breast cancer risk in postmenopausal women: Reanalysis of eighteen prospective studies. Steroids 99, 49–55 (2015).
https://doi.org/10.1016/j.steroids.2014.09.001 - Picon‐Ruiz, M., Morata‐Tarifa, C., Valle‐Goffin, J., Friedman, E. R. & Slingerland, J. M. Obesity and adverse breast cancer risk and outcome: Mechanistic insights and strategies for intervention. CA Cancer J. Clin. 67, 378–397 (2017).
https://doi.org/10.3322/caac.21405 - Gennari, A. et al. Impact of body mass index (BMI) on the prognosis of high-risk early breast cancer (EBC) patients treated with adjuvant chemotherapy. Breast Cancer Res. Treat. 159, 79–86 (2016).
https://doi.org/10.1007/s10549-016-3923-8 - Cecchini, R. S. 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).
https://doi.org/10.1158/1055-9965.EPI-15-0334-T - Chan, D. S. M. & Norat, T. Obesity and breast cancer: not only a risk factor of the disease. Curr. Treat. Options Oncol. 16, 22 (2015).
https://doi.org/10.1007/s11864-015-0341-9 - Trestini, I., Carbognin, L., Bonaiuto, C., Tortora, G. & Bria, E. The obesity paradox in cancer: clinical insights and perspectives. Eat. Weight Disord. 23, 185–193 (2018).
https://doi.org/10.1007/s40519-018-0489-y - Crozier, J. A. 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).
https://doi.org/10.1002/cncr.28051 - Yerushalmi, R. et al. Impact of baseline BMI and weight change in CCTG adjuvant breast cancer trials. Ann. Oncol. 28, 1560–1568 (2017).
https://doi.org/10.1093/annonc/mdx152 - Chan, D. S. M. et al. Body mass 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).
https://doi.org/10.1093/annonc/mdu042 - Ewertz, M. et al. Effect of obesity on prognosis after early-stage breast cancer. J. Clin. Oncol. 29, 25–31 (2011).
https://doi.org/10.1200/JCO.2010.29.7614 - Lee, K., Kruper, L., Dielie-Conwright, C. & Mortimer, J. The impact of obesity on breast cancer diagnosis and treatment. Curr. Oncol. Rep. 21 https://doi.org/10.1007/s11912-019-0787-1 (2019).
https://doi.org/10.1007/s11912-019-0787-1 - Yazici, O. et al. The effect of obesity on recurrence pattern in early breast cancer patients. J. Boun 20, 954–962 (2015).
- Garcia-Estevez, L. & Moreno-Bueno, G. Updating the role of obesity and cholesterol in breast cancer. Breast Cancer Res. 21, https://doi.org/10.1186/s13058-019-1124-1 (2019).
https://doi.org/10.1186/s13058-019-1124-1 - Bergom, C. et al. Association of locoregional control with high body mass index in women undergoing breast conservation therapy for early-stage breast cancer. Int J. Radiat. Oncol. Biol. Phys. 96, 65–71 (2016).
https://doi.org/10.1016/j.ijrobp.2016.04.020 - Pajares, B. 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–R105 (2013).
https://doi.org/10.1186/bcr3572 - Sparano, J. A. et al. Obesity at diagnosis is associated with inferior outcomes in hormone receptor-positive operable breast cancer. Cancer 118, 5937–5946 (2012).
https://doi.org/10.1002/cncr.27527 - Guo, Q. et al. Body mass index and breast cancer survival: a Mendelian randomization analysis. Int. J. Epidemiol. 46, 1814–1822 (2017).
https://doi.org/10.1093/ije/dyx131 - Sun, L., Zhu, Y., Qian, Q. & Tang, L. Body mass index and prognosis of breast cancer. Medicine 97, e11220 (2018).
https://doi.org/10.1097/MD.0000000000011220 - Renehan, A. G., Tyson, M., Egger, M., Heller, R. F. & Zwahlenm, M. Body-mass index and incidence of cancer: a systematic review and meta-analysis of prospective observational studies. Lancet 371, 569–578 (2008).
https://doi.org/10.1016/S0140-6736(08)60269-X - Klil-Drori, A. J., Azoulay, L. & Pollak, M. N. Cancer, obesity, diabetes, and antidiabetic drugs: is the fog clearing? Nat. Rev. Clin. Oncol. 14, 85–99 (2017).
https://doi.org/10.1038/nrclinonc.2016.120 - Lennon, H., Sperrin, M., Badrick, E. & Renehan, A. G. The obesity paradox in cancer: a review. Curr. Oncol. Rep. 18, 56 (2016).
https://doi.org/10.1007/s11912-016-0539-4 - Basen-Engquist, K. & Chang, M. Obesity and cancer risk: recent review and evidence. Curr. Oncol. Rep. 13, 71–76 (2011).
https://doi.org/10.1007/s11912-010-0139-7 - Lauby-Secretan, B. et al. Body fatness and cancer—viewpoint of the IARC Working Group. N. Engl. J. Med. 375, 794–798 (2016).
https://doi.org/10.1056/NEJMsr1606602 - Krasniqi, E. et al. Impact of BMI on HER2+ metastatic breast cancer patients treated with pertuzumab and/or trastuzumab emtansine. Real-world evidence. J. Cell. Physiol. 1–11, https://doi.org/10.1002/jcp.29445 (2020).
https://doi.org/10.1002/jcp.29445 - Dawood, S. et al. Prognostic value of body mass index in locally advanced breast cancer. J. Clin. Cancer Res. 14, 1718–1725, https://doi.org/10.1158/1078-0432.CCR-07-1479 (2008).
https://doi.org/10.1158/1078-0432.CCR-07-1479 - von Drygalski, A. et al. Obesity is an independent predictor of poor survival in metastatic breast cancer: retrospective analysis of a patient cohort whose treatment included high-dose chemotherapy and autologous stem cell support. Int. J. Breast Cancer 2011, 523276 (2011).
https://doi.org/10.4061/2011/523276 - Barba, M. et al. Body mass index and treatment outcomes in metastatic breast cancer patients treated with eribulin. J. Cell Physiol. 231, 986–991 (2016).
https://doi.org/10.1002/jcp.25213 - Pizzuti, L. et al. Body mass index in HER2-negative metastatic breast cancer treated with first-line paclitaxel and bevacizumab. Cancer Biol. Ther. 19, 328–334 (2018).
https://doi.org/10.1080/15384047.2017.1416938 - Martel, S. et al. Impact of body mass index on the clinical outcomes of patients with HER2-positive metastatic breast cancer. Breast 37, 142–147 (2018).
https://doi.org/10.1016/j.breast.2017.11.004 - Alarfi, H. et al. The impact of baseline body mass index on clinical outcomes in metastatic breast cancer: a prospective study. BMC Res. Notes 10, 550 (2017).
https://doi.org/10.1186/s13104-017-2876-2 - Parolin, V. et al Impact of BMI on clinical outcome of HER2-positive breast cancer. J. Clin. Oncol. 28, abstract 1130, https://doi.org/10.1200/jco.2010.28.15_suppl.1130 (2010).
https://doi.org/10.1200/jco.2010.28.15_suppl.1130 - Gennari, A. et al. Body mass index and prognosis of metastatic breast cancer patients receiving first-line chemotherapy. Cancer Epidemiol. Biomarkers Prev. 22, 1862–1867 (2013).
https://doi.org/10.1158/1055-9965.EPI-13-0595 - Franzoi, M. A. et al. Clinical implications of body mass index in metastatic breast cancer patients treated with abemaciclib and endocrine therapy. J Natl. Cancer Inst. https://doi.org/10.1093/jnci/djaa116 (2020).
https://doi.org/10.1093/jnci/djaa116 - Simkens, L. H. et al. Influence of body mass index on outcome in advanced colorectal cancer patients receiving chemotherapy with or without targeted therapy. Eur. J. Cancer 47, 2560–2567 (2011).
https://doi.org/10.1016/j.ejca.2011.06.038 - McQuade, J. L. et al. Association of body-mass index and outcomes in patients with metastatic melanoma treated with targeted therapy, immunotherapy, or chemotherapy: a retrospective, multicohort analysis. Lancet Oncol. 19, 310–322 (2018).
https://doi.org/10.1016/S1470-2045(18)30078-0 - Schneider, G., Kirschner, M. A., Berkowitz, R. & Ertel, N. H. Increased estrogen production in obese men. J. Clin. Endocrinol. Metab. 48, 633–638 (1979).
https://doi.org/10.1210/jcem-48-4-633 - Dhanapal, R., Saraswathi, T. & Govind, R. Cancer cachexia. J. Oral. Maxillofac. Pathol. 15, 257–260 (2011).
https://doi.org/10.4103/0973-029X.86670 - Meng, L. et al. Effect of early nutrition intervention on advanced nasopharyngeal carcinoma patients receiving chemoradiotherapy. J. Cancer 10, 3650–3656 (2019).
https://doi.org/10.7150/jca.33475 - Deluche, E. et al. Impact of body composition on outcome in patients with early breast cancer. Support Care Cancer 26, 861–868 (2018).
https://doi.org/10.1007/s00520-017-3902-6 - Maskarinec, G. et al. Factors affecting survival among women with breast cancer in Hawaii. J. Womens Health 20, 231–237 (2011).
https://doi.org/10.1089/jwh.2010.2114 - Kamineni, A. et al. Body mass index, tumor characteristics, and prognosis following diagnosis of early-stage breast cancer in a mammographically screened population. Cancer Causes Control 24, 305–312 (2013).
https://doi.org/10.1007/s10552-012-0115-7 - Faraoni, D. & Schaefer, S. T. Randomized controlled trials vs. observational studies: why not just live together? BMC Anesthesiol. 16, 102–102 (2016).
https://doi.org/10.1186/s12871-016-0265-3 - Flegal, K. M., Kruszon-Moran, D., Carroll, M. D., Fryar, C. D. & Ogden, C. L. Trends in obesity among adults in the United States, 2005 to 2014. Jama 315, 2284–2291 (2016).
https://doi.org/10.1001/jama.2016.6458 - Blair, C. K. et al. Obesity and survival among a cohort of breast cancer patients is partially mediated by tumor characteristics. npj Breast Cancer 5, 33 (2019).
https://doi.org/10.1038/s41523-019-0128-4 - VanderWeele, T. J. On the relative nature of overadjustment and unnecessary adjustment. Epidemiology. 20, 496–499 (2009).
https://doi.org/10.1097/EDE.0b013e3181a82f12 - Schisterman, E. F., Cole, S. R. & Platt, R. W. Overadjustment bias and unnecessary adjustment in epidemiologic studies. Epidemiology 20, 488–495 (2009).
https://doi.org/10.1097/EDE.0b013e3181a819a1 - Bradley, C., Given, C. & Roberts, C. Race, socioeconomic status, and breast cancer treatment and survival. J. Natl. Cancer Inst. 94, 490–496 (2002).
https://doi.org/10.1093/jnci/94.7.490 - Piccart-Gebhart, M. J. et al. Trastuzumab after adjuvant chemotherapy in HER2-positive breast cancer. N. Engl. J. Med. 353, 1659–1672 (2005).
https://doi.org/10.1056/NEJMoa052306 - Cameron, D. et al. 11 years’ follow-up of trastuzumab after adjuvant chemotherapy in HER2-positive early breast cancer: final analysis of the HERceptin adjuvant (HERA) trial. Lancet 389, 1195–1205 (2017).
https://doi.org/10.1016/S0140-6736(16)32616-2 - Swain, S. M. et al. Pertuzumab, trastuzumab, and docetaxel in HER2-positive metastatic breast cancer. N. Engl. J. Med. 372, 724–734 (2015).
https://doi.org/10.1056/NEJMoa1413513 - Swain, S. M. et al. Pertuzumab, trastuzumab, and docetaxel for HER2-positive metastatic breast cancer (CLEOPATRA study): overall survival results from a randomised, double-blind, placebo-controlled, phase 3 study. Lancet Oncol. 14, 461–471 (2013).
https://doi.org/10.1016/S1470-2045(13)70130-X - Baselga, J. et al. Pertuzumab plus trastuzumab plus docetaxel for metastatic breast cancer. N. Engl. J. Med. 366, 109–119 (2012).
https://doi.org/10.1056/NEJMoa1113216 - Perez, E. A. et al. Trastuzumab emtansine with or without pertuzumab versus trastuzumab plus taxane for human epidermal growth factor receptor 2-positive, advanced breast cancer: primary results from the phase III MARIANNE study. J. Clin. Oncol. 35, 141–148 (2016).
https://doi.org/10.1200/JCO.2016.67.4887 - Perez, E. A. et al. Phase III, randomized study of first-line trastuzumab emtansine (T-DM1) ± pertuzumab (P) vs. trastuzumab + taxane (HT) treatment of HER2-positive MBC: final overall survival (OS) and safety from MARIANNE. J. Clin. Oncol. 35, 1003–1003 (2017).
https://doi.org/10.1200/JCO.2017.35.15_suppl.1003 - Verma, S. et al. Trastuzumab emtansine for HER2-positive advanced breast cancer. N. Engl. J. Med. 367, 1783–1791 (2012).
https://doi.org/10.1056/NEJMoa1209124 - Diéras, V. et al. Trastuzumab emtansine versus capecitabine plus lapatinib in patients with previously treated HER2-positive advanced breast cancer (EMILIA): a descriptive analysis of final overall survival results from a randomised, open-label, phase 3 trial. Lancet Oncol. 18, 732–742 (2017).
https://doi.org/10.1016/S1470-2045(17)30312-1 - Krop, I. E. et al. Trastuzumab emtansine versus treatment of physician’s choice in patients with previously treated HER2-positive metastatic breast cancer (TH3RESA): final overall survival results from a randomised open-label phase 3 trial. Lancet Oncol. 18, 743–754 (2017).
https://doi.org/10.1016/S1470-2045(17)30313-3 - Krop, I. E. et al. Trastuzumab emtansine versus treatment of physician’s choice for pretreated HER2-positive advanced breast cancer (TH3RESA): a randomised, open-label, phase 3 trial. Lancet Oncol. 15, 689–699 (2014).
https://doi.org/10.1016/S1470-2045(14)70178-0 - Nuttall, F. Q. Body mass index: obesity, bmi, and health: a critical review. Nutr. Today 50, 117–128 (2015).
https://doi.org/10.1097/NT.0000000000000092 - Modi, N. D. et al. Metadata record for the manuscript: the obesity paradox in early and advanced HER2 positive breast cancer: pooled analysis of clinical trial data. figshare, https://doi.org/10.6084/m9.figshare.14046287 (2021).
https://doi.org/10.6084/m9.figshare.14046287
Публікації, які цитують цю публікацію
De novo Creation and Assessment of a Prognostic Fat-Age-Inflammation Index “FAIN” in Patients With Cancer: A Multicenter Cohort Study
Liangyu Yin, Chunhua Song, Jiuwei Cui, Xin Lin, Na Li, Yang Fan, Ling Zhang, Jie Liu, Feifei Chong, Chang Wang, Tingting Liang, Xiangliang Liu, Li Deng, Mei Yang, Jiami Yu, Xiaojie Wang, Xing Liu, Shoumei Yang, Zheng Zuo, Kaitao Yuan, Miao Yu, Minghua Cong, Zengning Li, Min Weng, Qinghua Yao, Pingping Jia, Suyi Li, Zengqing Guo, Wei Li, Hanping Shi, Hongxia Xu
https://doi.org/10.3389/fnut.2022.860285 ·
2022, Frontiers in Nutrition
Scopus
WoS
Цитувань Crossref:0
Multimodal Prediction of Five-Year Breast Cancer Recurrence in Women Who Receive Neoadjuvant Chemotherapy
Simona Rabinovici-Cohen, Xosé M. Fernández, Beatriz Grandal Rejo, Efrat Hexter, Oliver Hijano Cubelos, Juha Pajula, Harri Pölönen, Fabien Reyal, Michal Rosen-Zvi
https://doi.org/10.3390/cancers14163848 ·
2022, Cancers, №16, с.3848
Scopus
WoS
Цитувань Crossref:10
The obesity-breast cancer link: a multidisciplinary perspective
Emily N. Devericks, Meredith S. Carson, Lauren E. McCullough, Michael F. Coleman, Stephen D. Hursting
https://doi.org/10.1007/s10555-022-10043-5
2022, Cancer and Metastasis Reviews, №3, с.607-625
Scopus
WoS
Цитувань Crossref:21
Obesity and Dose of Anti-cancer Therapy: Are We Sure to Be on the Right Track in the Precision Medicine Era?
Tania Rossi, Erika Bandini, William Balzi, Francesco Fabbri, Ilaria Massa, Roberta Maltoni
https://doi.org/10.3389/fmed.2021.725346 ·
2021, Frontiers in Medicine
Scopus
WoS
Цитувань Crossref:0
Association between body mass index and incidence of breast cancer in premenopausal women: a Japanese nationwide database study
Takaaki Konishi, Michimasa Fujiogi, Nobuaki Michihata, Hiroki Matsui, Masahiko Tanabe, Yasuyuki Seto, Hideo Yasunaga
https://doi.org/10.1007/s10549-022-06638-9 ·
2022, Breast Cancer Research and Treatment, №2, с.315-325
Scopus
WoS
Цитувань Crossref:0
Exploring the Relationship between Obesity, Metabolic Syndrome and Neuroendocrine Neoplasms
Xiaoyang Lan, Nicola Fazio, Omar Abdel-Rahman
https://doi.org/10.3390/metabo12111150 ·
2022, Metabolites, №11, с.1150
Scopus
WoS
Цитувань Crossref:1
Racial Disparities in Clinical Outcomes on Investigator-Initiated Breast Cancer Clinical Trials at an Urban Medical Center
Jeffrey Aldrich, Princess Ekpo, Manali Rupji, Jeffrey M. Switchenko, Mylin A. Torres, Kevin Kalinsky, Manali A. Bhave
https://doi.org/10.1016/j.clbc.2022.10.005
2023, Clinical Breast Cancer, №1, с.38-44
Scopus
WoS
Цитувань Crossref:0
Association between high body mass index and prognosis of patients with early-stage breast cancer: A systematic review and meta-analysis
Zhoujuan Li, Guoshuang Shen, Mingqiang Shi, Yonghui Zheng, Yumei Guan, Yuanfang Xin, Miaozhou Wang, Fuxing Zhao, Dengfeng Ren, Jiuda Zhao
https://doi.org/10.1016/j.cpt.2023.03.002
2023, Cancer Pathogenesis and Therapy, №3, с.205-215
Scopus
Цитувань Crossref:2
Adherence to Cancer Prevention Lifestyle Recommendations Before, During, and 2 Years After Treatment for High-risk Breast Cancer
Rikki A. Cannioto, Kristopher M. Attwood, Evan W. Davis, Lucas A. Mendicino, Alan Hutson, Gary R. Zirpoli, Li Tang, Nisha M. Nair, William Barlow, Dawn L. Hershman, Joseph M. Unger, Halle C. F. Moore, Claudine Isaacs, Timothy J. Hobday, Gabriel N. Hortobagyi, Julie R. Gralow, Kathy S. Albain, G. Thomas Budd, Christine B. Ambrosone
https://doi.org/10.1001/jamanetworkopen.2023.11673 ·
2023, JAMA Network Open, №5, с.e2311673
Scopus
WoS
Цитувань Crossref:0
The prognostic impact of BMI in patients with HR+/HER2- advanced breast cancer: a study of the SONABRE registry
Senna W.M. Lammers, Hannah Thurisch, Ingeborg J.H. Vriens, Marissa Meegdes, Sanne M.E. Engelen, Frans L.G. Erdkamp, M. Wouter Dercksen, Birgit E.P.J. Vriens, Kirsten N.A. Aaldering, Manon J.A.E. Pepels, Linda M.H. van de Winkel, Natascha A.J.B. Peters, Jolien Tol, Joan B. Heijns, Agnes J. van de Wouw, Nathalie J.A. Teeuwen, Sandra M.E. Geurts, Vivianne C.G. Tjan-Heijnen
https://doi.org/10.21203/rs.3.rs-3156006/v1
2023
Цитувань Crossref:0
Знайти всі цитування публікації