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Estrogen concentrations in beef and human hormone-dependent cancers

2009; Elsevier BV; Volume: 20; Issue: 9 Linguagem: Inglês

10.1093/annonc/mdp381

1569-8041

Y Handa, H. Fujita, Sato Honma, Hisanori Minakami, Reiko Kishi,

Estrogen and related hormone effects

The recent increase of hormone-dependent cancers roughly parallels the increasing consumption of beef in Japan. During the past quarter century, hormone-dependent cancers have risen fivefold: 4 times in breast and ovarian cancer, 8 times in endometrial cancer, and 10 times in prostate cancer [1.Matsuda T. Marugame T. Kamo K. et al.Cancer incidence and incidence rates in Japan in 2002: based on data from 11 population-based cancer registries.Jpn J Clin Oncol. 2008; 38: 641-648Crossref PubMed Scopus (110) Google Scholar]. Meanwhile, popularization of the Western diet has resulted in a fivefold multiplication of beef consumption in Japan [2.General Food Policy Bureau, Ministry of Agriculture, Forestry and Fisheries of JapanFood Balance Sheet 2008; http://www.maff.go.jp/j/zyukyu/fbs/other/2-3-7.xls (29 June 2009, date last accessed)Google Scholar]. More than 25% of the beef has been imported from the United States [3.Ministry of Finance of JapanTrade Statistics of Japan. 2008; http://www.customs.go.jp/toukei/info/index.htm (29 June 2009, date last accessed)Google Scholar], where hormonal steroids including estradiol-17β have been implanted to cattle for growth promotion since the USA Food and Drug Administration approved the first steroid implant in 1956. In the USA, steroid implantation was carried out in 97% of beef cattle in 1999 [4.The USDA's National Animal Health Monitoring SystemChanges in the U.S. Feedlot Industry: 1994–1999-2000; http://www.aphis.usda.gov/vs/ceah/ncahs/nahms/feedlot/feedlot99/Fd99changes.pdf (29 June 2009, date last accessed)Google Scholar], though the practice is still uncommon in Japan. We conceived the possible relationship between estrogen concentrations in beef and incidence of hormone-dependent cancers and evaluated the levels of estradiol-17β (E2) and estrone (E1) in USA beef (fat: n = 40; red meat: n = 30) and Japanese beef (fat: n = 40; red meat: n = 30) by liquid chromatography–tandem mass spectrometry (LC-MS/MS; the lower sensitive limits for E2 and E1 were 0.1 and 0.5 pg, respectively) [5.Niikawa H. Suzuki T. Miki Y. et al.Intratumoral estrogens and estrogen receptors in human non-small cell lung carcinoma.Clin Cancer Res. 2008; 14: 4417-4426Crossref PubMed Scopus (176) Google Scholar]. The beef was raw sirloin steak sold as an ordinary grocery product at supermarkets in Sapporo city and obtained from tens of different stores at intervals of 3 weeks to avoid obtaining the same beef. Then, we measured estrogen concentrations in human uterine endometrial cancer (n = 50), ovarian cancer (n = 50), and normal controls (endometrium: n = 25; ovary: n = 25). We found that USA beef contained much higher levels of estrogen, particularly E2, than Japanese beef (Figure 1). The median concentrations (pg/g) of E2 and E1 in USA beef fat (14.0, 7.7) were 140 times and 11 times, respectively, higher than those in Japanese beef fat (0.1, 0.7). In red meat, E2 and E1 levels of USA beef (3.8, 1.0) were ∼600 times and 10 times, respectively, higher than those of Japanese beef (0.0, 0.1). Because steroid implant for cattle always contains E2 as a mixture, the elevated E2 levels in USA beef may have been ascribed to exogenous E2 residue resulting from steroid implantation. On the other hand, nearly zero level of E2 seen in Japanese beef was considered to be the natural endogenous status in beef without steroid implantation. E2 and E1 levels of endometrial cancer were higher in stage I (400.3, 133.5) and lower in stage III–IV (8.6, 34.7) than normal endometrium (203.9, 83.2). Ovarian cancer also showed higher levels in stage I (470.5, 527.6) and lower in stage III–IV (27.7, 36.3) than normal ovary (385.6, 156.4). The findings indicated that estrogen accumulation appears to play an initial role in the incidence of these cancers. Accordingly, it is our intuitive feeling that the increasing consumption of estrogen-rich beef following steroid implantation might facilitate estrogen accumulation in the human body and could be related to the incidence of hormone-dependent cancers. Although further studies are required to determine the relation for cancer incidence, we should be more aware of dietary estrogen intake from beef following steroid implantation and give mature consideration for the hormonal usage to livestock in the 21st century.