Abstract
Purpose
The Great Chinese Famine afflicted almost all Chinese people between 1959 and 1961. No study has explicitly assessed the association between an exposure to Chinese Famine and risk of overall breast cancer and tumor subtype. We evaluated the unique historical environmental influences of famine exposure on breast cancer subtypes.
Methods
16,469 Chinese women who were diagnosed with invasive breast cancer in the Fudan University Shanghai Cancer Center (FUSCC) from 1999 to 2014 were analyzed. Four tumor subtypes were defined by both estrogen-receptor (ER) and progesterone-receptor (PR) status. Multinomial logistic regression models were used to estimate the odds ratios (ORs) of ER−PR−, ER+PR−, and ER−PR+ relative to ER+PR+ breast cancer for exposure to famine and age at the exposure.
Results
Compared with cases not exposed to the Famine, exposed cases were more likely to be diagnosed with ER−PR− (OR 1.60, 95 % CI 1.43–1.81), ER−PR+ (OR 4.85, 95 % CI 3.80–6.19), and ER+PR− (OR 1.99, 95 % CI 1.67–2.37) than ER+PR+ breast cancer after controlling for established breast cancer risk factors. Women exposed to Famine after first birth had a higher risk of EP−PR− (OR 1.66, 95 % CI 1.28–2.15), ER−PR+ (OR 9.75, 95 % CI 5.85–16.25), and ER+PR− (OR 2.35, 95 % CI 1.69–3.26) compared to those with ER+PR+ breast cancer.
Conclusions
Women exposed to the Famine, particularly those exposed after first birth, were more likely to be diagnosed with ER−PR−, ER−PR+, and ER+PR− breast cancer. This retrospective analysis suggests that famine, malnutrition, or the associated lack of fruit and vegetable consumption in adulthood may be related to epidemiological heterogeneity within breast cancer subtypes.
Similar content being viewed by others
References
He M, Guo Q, Hu G (2011) Reversed urban-rural differences in breast cancer mortality (China, 2002–2008). Breast Cancer Res Treat 126(1):231–234
Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F (2015) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer J Int Du cancer 136(5):E359–E386
Fan L, Zheng Y, Yu KD, Liu GY, Wu J, Lu JS, Shen KW, Shen ZZ, Shao ZM (2009) Breast cancer in a transitional society over 18 years: trends and present status in Shanghai, China. Breast Cancer Res treat 117(2):409–416
Althuis MD, Fergenbaum JH, Garcia-Closas M, Brinton LA, Madigan MP, Sherman ME (2004) Etiology of hormone receptor-defined breast cancer: a systematic review of the literature. Cancer epidemiol, biomark prev 13(10):1558–1568
Xing P, Li J, Jin F (2010) A case-control study of reproductive factors associated with subtypes of breast cancer in Northeast China. Med Oncol 27(3):926–931
Yang XR, Chang-Claude J, Goode EL, Couch FJ, Nevanlinna H, Milne RL, Gaudet M, Schmidt MK, Broeks A, Cox A et al (2011) Associations of breast cancer risk factors with tumor subtypes: a pooled analysis from the Breast Cancer Association Consortium studies. J Natl Cancer Inst 103(3):250–263
Yu ZG, Jia CX, Geng CZ, Tang JH, Zhang J, Liu LY (2012) Risk factors related to female breast cancer in regions of Northeast China: a 1:3 matched case-control population-based study. Chin Med J 125(5):733–740
Linos E, Spanos D, Rosner BA, Linos K, Hesketh T, Qu JD, Gao YT, Zheng W, Colditz GA (2008) Effects of reproductive and demographic changes on breast cancer incidence in China: a modeling analysis. J Natl Cancer Inst 100(19):1352–1360
Lewington S, Li L, Murugasen S, Hong LS, Yang L, Guo Y, Bian Z, Collins R, Chen J, He H et al (2014) Temporal trends of main reproductive characteristics in ten urban and rural regions of China: the China Kadoorie biobank study of 300 000 women. Int J Epidemiol 43(4):1252–1262
DeSantis C, Ma J, Bryan L, Jemal A (2014) Breast cancer statistics, 2013. CA Cancer J Clin 64(1):52–62
Yao S (1999) A note on the causal factors of China’s famine in 1959–1961. J Polit Econ 107(6):1365–1369
Zhou X (2012) The great famine in China, 1958–1962: a documentary history, vol 137. Yale University Press, New Haven
van Abeelen AF, Veenendaal MV, Painter RC, de Rooij SR, Dijkgraaf MG, Bossuyt PM, Elias SG, Grobbee DE, Uiterwaal CS, Roseboom TJ (2012) Survival effects of prenatal famine exposure. Am J Clin Nutr 95(1):179–183
Wang N, Wang X, Li Q, Han B, Chen Y, Zhu C, Chen Y, Lin D, Wang B, Jensen MD et al (2015) The famine exposure in early life and metabolic syndrome in adulthood. Clin Nutr. doi:10.1016/j.clnu.2015.11.010
Wang N, Wang X, Han B, Li Q, Chen Y, Zhu C, Chen Y, Xia F, Cang Z, Zhu C et al (2015) Is exposure to famine in childhood and economic development in adulthood associated with diabetes? J Clin Endocrinol Metab 100(12):4514–4523
Wang Y, Wang X, Kong Y, Zhang JH, Zeng Q (2010) The great chinese famine leads to shorter and overweight females in chongqing chinese population after 50 years. Obesity 18(3):588–592
Elias SG, Peeters PH, Grobbee DE, van Noord PA (2005) The 1944–1945 dutch famine and subsequent overall cancer incidence. Cancer epidemiol, biomark prev 14(8):1981–1985
Elias SG, Peeters PH, Grobbee DE, van Noord PA (2004) Breast cancer risk after caloric restriction during the 1944–1945 dutch famine. J Natl Cancer Inst 96(7):539–546
Aune D, Chan DS, Vieira AR, Rosenblatt DA, Vieira R, Greenwood DC, Norat T (2012) Fruits, vegetables and breast cancer risk: a systematic review and meta-analysis of prospective studies. Breast Cancer Res Treat 134(2):479–493
Jung S, Spiegelman D, Baglietto L, Bernstein L, Boggs DA, van den Brandt PA, Buring JE, Cerhan JR, Gaudet MM, Giles GG et al (2013) Fruit and vegetable intake and risk of breast cancer by hormone receptor status. J Natl Cancer Inst 105(3):219–236
Wong IO, Schooling CM, Cowling BJ, Leung GM (2015) Breast cancer incidence and mortality in a transitioning Chinese population: current and future trends. Br J Cancer 112(1):167–170
Leung GM, Thach TQ, Lam TH, Hedley AJ, Foo W, Fielding R, Yip PS, Lau EM, Wong CM (2002) Trends in breast cancer incidence in Hong Kong between 1973 and 1999: an age-period-cohort analysis. Br J Cancer 87(9):982–988
Berkey CS, Gardner JD, Frazier AL, Colditz GA (2000) Relation of childhood diet and body size to menarche and adolescent growth in girls. Am J Epidemiol 152(5):446–452
Kung JKs, Lin JY (2003) The causes of china’s great leap famine, 1959–1961. Econ Dev Cult Change 52((1):51–73
Li LM (1981) Food and famine in China. Items 35(1–2):11–14
Lin JY, Yang DT (2000) Food availability, entitlements and the chinese famine of 1959–61. Econ J 110(460):136–158
Song S (2010) Mortality consequences of the 1959-1961 great leap forward famine in china: debilitation, selection, and mortality crossovers. Soc Sci Med 71(3):551–558
Kane P (1987) The demography of famine. Genus 43(1–2):43–58
Tamimi RM, Colditz GA, Hazra A, Baer HJ, Hankinson SE, Rosner B, Marotti J, Connolly JL, Schnitt SJ, Collins LC (2012) Traditional breast cancer risk factors in relation to molecular subtypes of breast cancer. Breast Cancer Res Treat 131(1):159–167
Baer HJ, Tworoger SS, Hankinson SE, Willett WC (2010) Body fatness at young ages and risk of breast cancer throughout life. Am J Epidemiol 171(11):1183–1194
Berkey CS, Willett WC, Tamimi RM, Rosner B, Frazier AL, Colditz GA (2013) Vegetable protein and vegetable fat intakes in pre-adolescent and adolescent girls, and risk for benign breast disease in young women. Breast Cancer Res Treat 141(2):299–306
Bae JM (2016) Reinterpretation of the results of a pooled analysis of dietary carotenoid intake and breast cancer risk by using the interval collapsing method. Epidemiol Health 38:e2016024
Boeke CE, Tamimi RM, Berkey CS, Colditz GA, Eliassen AH, Malspeis S, Willett WC, Frazier AL (2014) Adolescent carotenoid intake and benign breast disease. Pediatrics 133(5):e1292–e1298
Hendrickson SJ, Willett WC, Rosner BA, Eliassen AH (2013) Food predictors of plasma carotenoids. Nutrients 5(10):4051–4066
Zhang X, Spiegelman D, Baglietto L, Bernstein L, Boggs DA, van den Brandt PA, Buring JE, Gapstur SM, Giles GG, Giovannucci E et al (2012) Carotenoid intakes and risk of breast cancer defined by estrogen receptor and progesterone receptor status: a pooled analysis of 18 prospective cohort studies. Am J Clin Nutr 95(3):713–725
Eliassen AH, Hendrickson SJ, Brinton LA, Buring JE, Campos H, Dai Q, Dorgan JF, Franke AA, Gao YT, Goodman MT et al (2012) Circulating carotenoids and risk of breast cancer: pooled analysis of eight prospective studies. J Natl Cancer Inst 104(24):1905–1916
Colditz GA, Rosner BA, Chen WY, Holmes MD, Hankinson SE (2004) Risk factors for breast cancer according to estrogen and progesterone receptor status. J Natl Cancer Inst 96(3):218–228
Ma H, Bernstein L, Ross RK, Ursin G (2006) Hormone-related risk factors for breast cancer in women under age 50 years by estrogen and progesterone receptor status: results from a case–control and a case–case comparison. Breast Cancer 8(4):R39
Sisti JS, Collins LC, Beck AH, Tamimi RM, Rosner BA, Eliassen AH (2015) Reproductive risk factors in relation to molecular subtypes of breast cancer: Results from the Nurses’ Health Studies. Int J Cancer J Int Du Cancer. doi:10.1002/ijc.29968
Acknowledgments
The authors thank the Shanghai Cancer Hospital for supplying the aggregate data, and Foundation for Barnes-Jewish Hospital for funding this study funds. GAC and YL are also supported by the Breast Cancer Research Foundation. Shanghai Hospital collected data through operation of its tumor registry. This is an international collaboration between Washington University School of Medicine and Fudan University Shanghai Cancer Center.
Funding
Supported by funds from the Foundation for Barnes-Jewish Hospital and Fudan University Shanghai Cancer Center. GAC and YL were also supported by the Breast Cancer Research Foundation. The funders had no role in study design, data collection, analysis, interpretation of data, preparation of the report, or decision to publish. All authors had full access to all the data and analyses and had final responsibility for the decision to submit for publication.
Authors contribution
AA, GAC, and YL contributed to the design of the study. ZMS GYL, MM JW ZZS, and NSH contributed to data collection. AA, YL, MM, and WHX contributed to data review. AA and YL contributed to data analysis. AA, GAC, and YL contributed to data interpretation. AA, GAC, and YL contributed to the writing and revision of the report. AA searched the scientific literature, produced the figures and tables, and drafted the manuscript. GAC and YL contributed to the critical revision of the paper. All authors (AA, MM, YL, NSH, GYL, WHX, JW, ZZS, ZMS, and GAC) contributed to the review of the report and approved the final submitted version.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Appendix
Appendix
See Table 4.
Rights and permissions
About this article
Cite this article
Alimujiang, A., Mo, M., Liu, Y. et al. The association between China’s Great famine and risk of breast cancer according to hormone receptor status: a hospital-based study. Breast Cancer Res Treat 160, 361–369 (2016). https://doi.org/10.1007/s10549-016-3994-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10549-016-3994-6