Possibility of breast cancer prevention: Use of soy isoflavones and fermented soy beverage produced using probiotics

International Journal of Molecular Sciences

Volumn 16, Issue 5, 2015, Pages 10907-10920

  Takagi, Akimitsu ^a   Kano, Mitsuyoshi ^a   Kaga, Chiaki ^a  

^a YAKULT CENTRAL INSTITUTE FOR MICROBIOLOGICAL RESEARCH   (Japan)

Author keywords

Breast cancer; Fermented soy milk; Isoflavone; L. casei Shirota; Probiotics

Indexed keywords

ISOFLAVONE DERIVATIVE; PROBIOTIC AGENT; SOY ISOFLAVONE; UNCLASSIFIED DRUG;

BEVERAGE; BREAST CANCER; CANCER PREVENTION; CARCINOGENESIS; FERMENTATION; HUMAN; INCIDENCE; LIFESTYLE; NONHUMAN; REVIEW; RISK FACTOR; SOYBEAN MILK; TUMOR VOLUME; BREAST NEOPLASMS; CHEMISTRY; FEMALE; SOYBEAN;

GLYCINE MAX;

BREAST NEOPLASMS; FEMALE; FERMENTATION; HUMANS; ISOFLAVONES; PROBIOTICS; SOY MILK; SOYBEANS;

EID: 84929376644     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms160510907     Document Type: Review

References (60)

1. Scheiber, M.D.; Liu, J.H.; Subbiah, M.T.; Rebar, R.W.; Setchell, K.D. Dietary inclusion of whole soy foods results in significant reductions in clinical risk factors for osteoporosis and cardiovascular disease in normal postmenopausal women. Menopause 2001, 8, 384–392.
2. Messina, M.J.; Persky, V.; Setchell, K.D.; Barnes, S. Soy intake and cancer risk: A review of the in vitro and in vivo data. Nutr. Cancer 1994, 21, 113–131.
3. Setchell, K.D.; Cassidy, A. Dietary isoflavones: Biological effects and relevance to human health. J. Nutr. 1999, 129, 758S–767S.
4. Molteni, A.; Brizio-Molteni, L.; Persky, V. In vitro hormonal effects of soybean isoflavones. J. Nutr. 1995, 125, 751S–756S.
5. Akiyama, T.; Ishida, J.; Nakagawa, S.; Ogawara, H.; Watanabe, S.; Itoh, N.; Shibuya, M.; Fukami, Y. Genistein, a specific inhibitor of tyrosine-specific protein kinases. J. Biol. Chem. 1987, 262, 5592–5595.
6. Su, S.J.; Yeh, T.M.; Chuang, W.J.; Ho, C.L.; Chang, K.L.; Cheng, H.L.; Liu, H.S.; Cheng, H.L.; Hsu, P.Y.; Chow, N.H. The novel targets for anti-angiogenesis of genistein on human cancer cells. Biochem. Pharmacol. 2005, 69, 307–318.
7. Guo, T.L.; McCay, J.A.; Zhang, L.X.; Brown, R.D.; You, L.; Karrow, N.A.; Germolec, D.R.; White, K.L. Jr. Genistein modulates immune responses and increases host resistance to B16F10 tumor in adult female B6C3F1 mice. J. Nutr. 2001, 131, 3251–3258.
8. Dijsselbloem, N.; Vanden, B.W.; De, N.A.; Haegeman, G. Soy isoflavone phyto-pharmaceuticals in interleukin-6 affections. Multi-purpose nutraceuticals at the crossroad of hormone replacement, anti-cancer and anti-inflammatory therapy. Biochem. Phamacol. 2004, 68, 1171–1185.
9. Husain, D.; Khanna, K.; Puri, S.; Haghighizadeh, M. Supplementation of soy isoflavones improved sex hormones, blood pressure, and postmenopausal symptoms. J. Am. Coll. Nutr. 2015, 34, 42–48.
10. Wangen, K.E.; Duncan, A.M.; Xu, X.; Kurzer, M.S. Soy isoflavones improve plasma lipids in normocholesterolemic and mildly hypercholesterolemic postmenopausal women. Am. J. Clin. Nutr. 2001, 73, 225–231.
11. Lagari, V.S.; Levis, S. Phytoestrogens in the prevention of postmenopausal bone loss. J. Clin. Densitom. 2013, 16, 445–449.
12. Lethaby, A.; Marjoribanks, J.; Kronenberg, F.; Roberts, H.; Eden, J.; Brown, J. Phytoestrogens for menopausal vasomotor symptoms. Cochrane Database Syst. Rev. 2013, 10, CD001395.
13. Nagata, C.; Mizoue, T.; Tanaka, K.; Tsuji, I.; Tamakoshi, A.; Matsuo, K.; Wakai, K.; Inoue, M.; Tsugane, S.; Sasazuki, S., et al. Soy intake and breast cancer risk: An evaluation based on a systematic review of epidemiologic evidence among the Japanese population. Jpn. J. Clin. Oncol. 2014, 44, 282–295.
14. Xie, Q, Chen, M.L.; Qin, Y.; Zhang, Q.Y.; Xu, H.X.; Zhou, Y.; Mi, M.T.; Zhu, J.D. Isoflavone consumption and risk of breast cancer: A dose-response meta-analysis of observational studies. Asia Pac. J. Clin. Nutr. 2013, 22, 118–127.
15. Wang, H.G.; Murphy, P.A. Isoflavone content in commercial soybean foods. J. Agric. Food Chem. 1994, 42, 1666–1673.
16. Coward, L.; Barnes, N.C.; Setchell, K.D.R.; Barnes, S. Genistein, daidzein and their β-glycocide conjugates: Antitumor isoflavones in soybean foods from American and Asian diets. J. Agric. Food Chem. 1993, 41, 1961–1967.
17. Setchell, K.D.; Brown, N.M.; Zimmer-Nechemias, L.; Brashear, W.T.; Wolfe, B.E.; Kirschner, A.S.; Heubi, J.E. Evidence for lack of absorption of soy isoflavone glycosides in humans, supporting the crucial role of intestinal metabolism for bioavailability. Am. J. Clin. Nutr. 2002, 76, 447–453.
18. Atkinson, C.; Frankenfeld, C.L.; Lampe, J.W. Gut bacterial metabolism of the soy isoflavone daidzein: Exploring the relevance to human health. Exp. Biol. Med. (Maywood) 2005, 230, 155–170.
19. Bressani, R.; Elías, L.G. Processed vegetable protein mixtures for human consumption in developing countries. Adv. Food Res. 1968, 66, 1–103.
20. Murti, T.W.; Bouillanne, C.; Landon, M.; Desmazeaud, M.J. Bacterial growth and volatile compounds in yoghurt-type products from soymilk containing Bifidobacterium spp. J. Food Sci. 1992, 1, 153–157.
21. Shimakawa, Y.; Matsubara, S.; Yuki, N.; Ikeda, M.; Ishikawa, F. Evaluation of Bifidobacterium breve strain Yakult-fermented soymilk as a probiotic food. Int. J. Food Microbiol. 2003, 81, 131–136.
22. Chien, H.L.; Huang, H.Y.; Chou, C.C. Transformation of isoflavone phytoestrogens during the fermentation of soymilk with lactic acid bacteria and bifidobacteria. Food Microbiol. 2006, 23, 772–778.
23. Kano, M.; Takayanagi, T.; Harada, K.; Sawada, S.; Ishikawa, F. Bioavailability of isoflavones after ingestion of soy beverages in healthy adults. J. Nutr. 2006, 136, 2291–2296.
24. Kano, M.; Ishikawa, F. Nutrition and Alcohol—Linking Nutrient Interactions and Dietary Intake; Watson, R., Preedy, V.R., Eds.; CRC Press: New York, NY, USA, 2004; pp. 301–311.
25. Kano, M.; Ishikawa, F.; Matsubara, S.; Kikuchi-Hayakawa, H.; Shimakawa, Y. Soymilk products affect ethanol absorption and metabolism in rats during acute and chronic ethanol intake. J. Nutr. 2002, 132, 238–244.
26. Kikuchi-Hayakawa, H.; Onodera, N.; Matsubara, S.; Yasuda, E.; Chonan, O.; Talahashi, R.; Ishikawa, F. Effects of soy milk and Bifidobacterium fermented soy milk on lipid metabolism in aged ovariectomized rats. Biosci. Biotechnol. Biochem. 1998, 62, 1688–1692.
27. Kikuchi-Hayakawa, H.; Onodera, N.; Matsubara, S.; Yasuda, E.; Shimakawa, Y.; Takahashi, R.; Ishikawa, F. Effects of soya milk and Bifidobacterium-fermented soya milk on plasma and liver lipids, and faecal steroids in hamsters fed on a cholesterol-free or cholesterol-enriched diet. Br. J. Nutr. 1998, 79, 97–105.
28. Kikuchi-Hayakawa, H.; Onodera-Masuoka, N.; Kano, M.; Matsubara, S.; Yasuda, E.; Ishikawa, F. Effect of soy milk and Bifidobacterium-fermented soy milk on plasma and liver lipids in ovariectomized syrian hamsters. J. Nutr. Sci. Vitaminol. 2000, 46, 105–108.
29. Anderson, B.O.; Jakesz, R. Breast cancer issues in developing countries: An overview of the Breast Health Global Initiative. World J. Surg. 2008, 32, 2578–2585.
30. Hirabayashi, Y.; Zhang, M. Comparison of time trends in breast cancer incidence (1973–2002) in Asia, from cancer incidence in five continents, Vols IV-IX. Jpn. J. Clin. Oncol. 2009, 39, 411–412.
31. Shin, H.R.; Boniol, M.; Joubert, C.; Hery, C.; Haukka, J.; Autier, P.; Nishino, Y.; Sobue, T.; Chen, C.J.; You, S.L., et al. Secular trends in breast cancer mortality in five East Asian populations: Hong Kong, Japan, Korea, Singapore and Taiwan. Cancer Sci. 2010, 101, 1241–1246.
32. About Cancer Statistics in Japan 2009. Center for Cancer controland information services, National Cancer Center. Available online: http://ganjoho.ncc.go.jp/public/statistics/backnumber/2009_en.html (accessed on 21. February 2011).
33. Harkinson, S.; Tamimi, R.; Hunter, D. Textbooks of cancer epidemiology, 2nd Edition; Adami, H.O., Hunter, D.; Trichopoulos, D., Eds.; Oxford University Press: New York, NY, USA, 2008; Chapter 16.
34. Nagata, C.; Kawakami, N.; Shimizu, H. Trends in the incidence rate and risk factors for breast cancer in Japan. Breast Cancer Res. Treat. 1997, 44, 75–82.
35. Amine, E.K.; Baba, N.H.; Belhadj, M.; Deurenberg-Yap, M.; Djazayery, A.; Forrester, T.; Galuska, D.A.; Herman, S.; James, W.P.T.; M’Buyamba Kabangu, J.R. et al. Report of A Joint WHO/FAO Expert Consultation. Diet, Nutrition, and the Prevention of Chronic Diseases, WHO Technical Report Series 916. Presented at World Health Organization, Geneva, Switzerland, 28. January–1. February 2002.
36. Parkin, S.L.; Whelan, S.L.; Ferlay, J.; Teppo, L.; Thomas, D.B. (Eds.) Cancer Incidence in Five Contrinents Vol VIII; IARC Scientific Publications: Lyon, France, 2002; No. 155.
37. Toi, M.; Hirota, S.; Tomotaki, A.; Sato, N.; Nozumi, Y.; Anan, K.; Nagashima, T.; Tokuda, Y.; Masuda, N.; Ohsumi, N. et al. Probiotic beverage with soy isoflavone consumption for breast cancer prevention: A case-control study. Curr. Nutr. Food Sci. 2013, 9, 194–200.
38. Aso, Y.; Akaza, H.; Kotake, T.; Tsukamoto, T.; Imai, K.; Naito, S. Preventive effect of a Lactobacillus casei preparation on the recurrence of superficial bladder cancer in a double-blind trial. The BLP Study Group. Eur. Urol. 1995, 27, 104–109.
39. Ohashi, Y.; Nakai, S.; Tsukamoto, T.; Masumori, N.; Akaza, H.; Miyanaga, N.; Kitamura, T.; Kawabe, K.; Kotake, T.; Kuroda, M. et al. Habitual intake of lactic acid bacteria and risk reduction of bladder cancer. Urol. Int. 2002, 68, 273–280.
40. Naito, S.; Koga, H.; Yamaguchi, A.; Fujimoto, N.; Hasui, Y.; Kuramoto, H.; Iguchi, A.; Kinukawa, N.; Kyushu University Urological Oncology Group. Prevention of recurrence with epirubicin and Lactobacillus casei after transurethral resection of bladder cancer. J. Urol. 2008, 179, 485–490.
41. Ishikawa, H.; Akedo, I.; Otani, T.; Suzuki, T.; Nakamura, T.; Takeyama, I.; Ishiguro, S.; Miyaoka, E.; Sobue, T.; Kakizoe, T. Randomized trial of dietary fiber and Lactobacillus casei administration for prevention of colorectal tumors. Int. J. Cancer 2005, 116, 762–767.
42. De Moreno de LeBlanc, A.; Matar, C.; LeBlanc, N.; Perdigón, G. Effects of milk fermented by Lactobacillus helveticus R389 on a murine breast cancer model. Breast Cancer Res. 2005, 7, R477–R486.
43. Takagi, A.; Ikemura, H.; Matsuzaki, T.; Sato, M.; Nomoto, K.; Morotomi, M.; Yokokura, T. Relationship between the in vitro response of dendritic cells to Lactobacillus and prevention of tumorigenesis in the mouse. J. Gastroenterol. 2008, 43, 661–669.
44. Lai, L.R.; Hsieh, S.C.; Huang, H.Y.; Chou, C.C. Effect of lactic fermentation on the total phenolic, saponin and phytic acid contents as well as anti-colon cancer cell proliferation activity of soymilk. J. Biosci. Bioeng. 2013, 115, 552–556.
45. Chang, W.H.; Liu, J.J.; Chen, C.H.; Huang, T.S.; Lu, F.J. Growth inhibition and induction of apoptosis in MCF-7 breast cancer cells by fermented soy milk. Nutr. Cancer 2002, 43, 214–226.
46. Ohta, T.; Nakatsugi, S.; Watanabe, K.; Kawamori, T.; Ishikawa, F.; Morotomi, M.; Sugie, S.; Toda, T.; Sugimura, T.; Wakabayashi, K. Inhibitory effects of Bifidobacterium-fermented soy milk on 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine-induced rat mammary carcinogenesis, with a partial contribution of its component isoflavones. Carcinogenesis 2000, 21, 937–941.
47. Kaga, C.; Takagi, A.; Kano, M.; Kado, S.; Kato, I.; Sakai, M.; Miyazaki, K.; Nanno, M.; Ishikawa, F.; Ohashi, Y. et al. Lactobacillus casei Shirota enhances the preventive efficacy of soymilk in chemically induced breast cancer. Cancer Sci. 2013, 104, 1508–1514.
48. Takagi, A.; Matsuzaki, T.; Sato, M.; Nomoto, K.; Morotomi, M.; Yokokura, T. Enhancement of natural killer cytotoxicity delayed murine carcinogenesis by a probiotic microorganism. Carcinogenesis 2001, 22, 599–605.
49. Nagao, F.; Nakayama, M.; Muto, T.; Okumura, K. Effects of a fermented milk drink containing Lactobacillus casei strain Shirota on the immune system in healthy human subjects. Biosci. Biotechnol. Biochem. 2000, 64, 2706–2708.
50. Dong, H.; Rowland, I.; Thomas, L.V.; Yaqoob, P. Immunomodulatory effects of a probiotic drink containing Lactobacillus casei Shirota in healthy older volunteers. Eur. J. Nutr. 2013, 52, 1853–1863.
51. Reale, M.; Boscolo, P.; Bellante, V.; Tarantelli, C.; di Nicola, M.; Forcella, L.; Li, Q.; Morimoto, K.; Muraro, R. Daily intake of Lactobacillus casei Shirota increases natural killer cell activity in smokers. Br. J. Nutr. 2012, 108, 308–314.
52. Kaga, C.; Takagi, A.; Kano, M. Chemopreventive effect of soymilk fermented with probiotics. In Preparation.
53. Fritz, H.; Seely, D.; Flower, G.; Skidmore, B.; Fernandes, R.; Vadeboncoeur, S.; Kennedy, D.; Cooley, K.; Wong, R.; Sagar, S. et al. Soy, red clover, and isoflavones and breast cancer: A systematic review. PLoS ONE 2013, 8, e81968.
54. Yamori, Y. Food factors for atherosclerosis prevention: Asian perspective derived from analyses of worldwide dietary biomarkers. Exp. Clin. Cardiol. 2006, 11, 94–98.
55. Shu, X.O.; Zheng, Y.; Cai, H.; Gu, K.; Chen, Z.; Zheng, W.; Lu, W. Soy food intake and breast cancer survival. JAMA 2009, 302, 2437–2443.
56. Matsuno, R.K; Anderson, W.F.; Yamamoto, S.; Tsukuma, H.; Pfeiffer, R.M.; Kobayashi, K.; Devesa, S.S.; Levine, P.H. Early- and late-onset breast cancer types among women in the United States and Japan. Cancer Eprdemiol. Biomark. Prev. 2007, 16, 1437–1442.
57. Prentice, R.L.; Garnet L. The women’s health initiative: Lessons learned. Ann. Rev. Public Health 2008, 29, 131–150.
58. Prentice, R.L.; Caan, B.; Chlebowski, R.T.; Patterson, R.; Kuller, L.H.; Ockene J.K.; Margolis, K.L.; Limacher, M.C.; Manson, J.E.; Parker, L.M. et al. Low-fat dietary pattern and risk of invasive breast cancer: The women’s health initiative randomized controlled dietary modification trial. JAMA 2006, 295, 629–642.
59. Martin, L.J.; Li, Q.; Melnichouk, O.; Greenberg, C.; Minkin, S.; Hislop, G.; Boyd, N.F. A randomized trial of dietary intervention for breast cancer prevention. Cancer Res. 2011, 71, 123–133.
60. Chlebowski, R.T.; Blackburn, G.L.; Thomson, C.A.; Nixon, D.W.; Shapiro, A.; Hoy, M.K.; Goodman, M.T.; Giuliano, A.E.; Karanja, N.; McAndrew, P. et al. Dietary fat reduction and breast cancer outcome: Interim efficacy results from the women’s intervention nutrition study. J. Natl. Cancer Inst. 2006, 98, 1767–1776.