Asian Pacific Journal of Cancer Prevention

Asian Pacific Journal of Cancer Prevention (아시아태평양암예방학회)
권호 표지

Mate and Tea Intake, Dietary Antioxidants and Risk of Breast Cancer: a Case-Control Study

  • Ronco, Alvaro L (Unit of Oncology and Radiotherapy, Pereira Rossell Women's Hospital) ;
  • Stefani, Eduardo De (Pathology Department, Clinical Hospital, UDELAR State University) ;
  • Mendoza, Beatriz (Endocrinology and Metabolism Department, Clinical Hospital, UDELAR State University) ;
  • Vazquez, Alvaro (Biomedical Sciences Center, University of Montevideo) ;
  • Abbona, Estela (Nutrition Department, Pereira Rossell Women's Hospital) ;
  • Sanchez, Gustavo (Endocrinology and Metabolism Department, Clinical Hospital, UDELAR State University) ;
  • Rosa, Alejandro De (Unit of Oncology and Radiotherapy, Pereira Rossell Women's Hospital)
  • Published : 2016.06.01
⟨ Previous Next ⟩

Abstract

Recently, we reported an inverse association between high 'mate' intake (infusion of Ilex paraguariensis herb, a staple beverage in temperate South America) and breast cancer (BC) risk. Stronger inverse associations were found in high strata of tea, vegetable, fruit and energy intakes, and in overweight/obese women, suggesting possible roles for 'mate' mainly from its antioxidant contribution. The present study attempted to thoroughly explore possible associations among 'mate' and tea intake, dietary antioxidants and BC risk. Combining two databases of previous studies, 572 BC incident cases and 889 controls were interviewed with a specific questionnaire featuring socio-demographic, reproductive and lifestyle variables, and a food frequency questionnaire (64 items), focusing on 'mate' intake (consumer status, daily intake, age at start, age at quit, duration of habit). Food-derived nutrients were calculated from available databases. Odds ratios (OR) and their 95% confidence intervals were calculated through unconditional logistic regression, adjusting for relevant potential confounders. The highest 'mate' intake was significantly inversely associated with BC risk for both low and high carotenoids (OR=0.40 vs. 0.41), vitamin C (OR=0.33 vs. 0.50), vitamin E (OR=0.37 vs. 0.45), flavonols (OR=0.38 vs. 0.48) and reduced glutathione (OR=0.48 vs. 0.46) strata. High tea intake showed significant inverse risk associations only with high carotenoids (OR=0.41), vitamin E (OR=0.48) and reduced glutathione (OR=0.43) strata. In conclusion, a strong and inverse association for 'mate' intake and BC was found, independent of dietary antioxidant levels. Also strong inverse associations with tea intake were more evident only at high levels of certain dietary antioxidants.

Keywords

References

  1. Allouche Y, Warleta F, Campos M, et al (2010). Antioxidant, antiproliferative, and pro-apoptotic capacities of pentacyclic triterpenes found in the skin of olives on MCF-7 human breast cancer cells and their effects on DNA damage. J Agr Food Chem, 59, 121-30.
  2. Badal S, Delgada R (2014). Role of the modulation of CYP1A1 expression and activity in chemoprevention. J Appl Toxicol, 34, 743-53. https://doi.org/10.1002/jat.2968
  3. Barrios E, Garau M, Alonso R, Musetti C (2014). IV Atlas of cancer incidence in uruguay. comision honoraria de lucha contra el cancer, montevideo, uruguay. (in Spanish)
  4. Bhagwat S, Haytowitz DB, Holden JM. U.S. Dept. of Agriculture (2013). Database for the Flavonoid Content of Selected Foods, Release 3.1. Beltsville, Maryland.
  5. Bhoo-Pathy N, Peeters PH, Uiterwaal CS, et al (2015). Coffee and tea consumption and risk of pre- and postmenopausal breast cancer in the european prospective investigation into cancer and nutrition (EPIC) cohort study. Breast Cancer Res, 17, 15-26. https://doi.org/10.1186/s13058-015-0521-3
  6. Bishayee A, Ahmed S, Brankov A, Perloff M (2011). Triterpenoids as potential agents for the chemoprevention and therapy of breast cancer. Front Biosci, 16, 980-96. https://doi.org/10.2741/3730
  7. Bracesco N, Sanchez AG, Contreras V, et al (2011). Recent advances on Ilex paraguariensis research: minireview. J Ethnopharmacol, 136, 378-84. https://doi.org/10.1016/j.jep.2010.06.032
  8. Breslow NE, Day NE (1980). Statistical methods in cancer research: Volume 1. The analysis of case-control studies. Int Agency Res Cancer Sci Pub, 32, Lyon, France.
  9. Butt MS, Imram A, Sharif MK, et al (2014). Black tea polyphenols: a mechanistic treatise. Crit Rev Food Sci Nutr, 54, 1002-11. https://doi.org/10.1080/10408398.2011.623198
  10. Cavalieri E, Frenkel K, Liehr JG, Rogan E, Roy D (2000). Estrogens as endogenous genotoxic agents-DNA adducts and mutations. J Natl Cancer Inst Monogr, 27, 75-93.
  11. Chakravarti B, Maurya R, Siddiqui JA, et al (2012). In vitro anti-breast cancer activity of ethanolic extract of Wrightia tomentosa: role of pro-apoptotic effects of oleanolic acid and ursolic acid. J Ethnopharmacol, 142, 72-9. https://doi.org/10.1016/j.jep.2012.04.015
  12. Chumsri S, Howes T, Bao T, Sabnis G, Brodie A (2011). Aromatase, aromatase inhibitors, and breast cancer. J Steroid Biochem Mol Biol, 125, 13-22. https://doi.org/10.1016/j.jsbmb.2011.02.001
  13. Comision Honoraria de Lucha Contra el Cancer (1993). Knowledge, beliefs, attitudes and practices related to cancer: population survey. Technical cooperation PNUD/BID. comision honoraria de lucha contra el cancer, montevideo, uruguay. (in Spanish)
  14. Coppes Z, Escardo C, Pavlisko A, Leonard SS (2014). Antioxidant properties of Yerba Mate tea and its inhibition of radical DNA damage, and comparison with other types of tea. Proceedings of the VI South American Congress on Yerba Mate, Montevideo. Abst.150. p.194.
  15. De Angel RE, Smith SM, Glickman RD, Perkins SN, Hursting SD (2010). Antitumor effects of ursolic acid in a mouse model of postmenopausal breast cancer. Nutr Cancer, 62, 1074-86. https://doi.org/10.1080/01635581.2010.492092
  16. De Stefani E, Correa P, Fierro L, et al (1991). Black tobacco, mate, and bladder cancer. A case-control study from Uruguay. Cancer, 67, 536-40. https://doi.org/10.1002/1097-0142(19910115)67:2<536::AID-CNCR2820670236>3.0.CO;2-8
  17. De Stefani E, Fierro L, Mendilaharsu M, et al (1998). Meat intake, "mate" drinking and renal cell cancer in Uruguay. A case-control study. Br J Cancer, 78, 1239-43. https://doi.org/10.1038/bjc.1998.661
  18. De Stefani E, Moore M, Aune D, et al (2011). Mate consumption and risk of cancer: a multi-site case-control study in Uruguay. Asian Pac J Cancer Prev, 12, 1089-93.
  19. Es-Saady D, Simon A, Jayat-Vignoles C, et al (1995). MCF-7 cell cycle arrested at G1 through ursolic acid, and increased redction of tetrazolium salts. Anticancer Res, 16, 481-6.
  20. Feig SA (1999). Role and evaluation of mammography and other imaging methods for breast cancer detection, diagnosis, and staging. Semin Nucl Med, 29, 3-15. https://doi.org/10.1016/S0001-2998(99)80026-9
  21. Felty Q, Xiong WC, Sun D, et al (2005a). Estrogen-induced mitochondrial reactive oxygen species as signal-transducing messengers. Biochemistry, 44, 6900-9. https://doi.org/10.1021/bi047629p
  22. Felty Q, Singh KP, Roy D (2005b). Estrogen-induced G1/S transition of G0-arrested estrogen-dependent breast cancer cells is regulated by mitochondrial oxidant signalling. Oncogene, 24, 4883-93. https://doi.org/10.1038/sj.onc.1208667
  23. Ferlay J, Soerjomataram I, Ervik M, et al (2013). GLOBOCAN 2012 v1.0, Cancer incidence and mortality worldwide: IARC CancerBase No. 11 [Internet]. Lyon, France: International Agency for Research on Cancer.
  24. Gao Y, Huang YB, Liu XO, et al (2013). Tea Consumption, Alcohol Drinking and Physical Activity Associations with Breast Cancer Risk among Chinese Females: a Systematic Review and Meta-analysis. Asian Pac J Cancer Prev, 14, 7543-50. https://doi.org/10.7314/APJCP.2013.14.12.7543
  25. Gierach GL, Freedman ND, Andaya A, et al (2012). Coffee intake and breast cancer risk in the NIH-AARP diet and health study cohort. Int J Cancer, 131, 452-60. https://doi.org/10.1002/ijc.26372
  26. Gnoatto SCB, Dassonville-Klimpt A, Da Nascimento S, et al (2008). Evaluation of ursolic acid isolated from Ilex paraguariensis and derivatives on aromatase inhibition. Eur J Med Chem, 43, 1865-77. https://doi.org/10.1016/j.ejmech.2007.11.021
  27. Heck CI, de Mejia EG (2007). Yerba Mate Tea (Ilex paraguariensis): a comprehensive review on chemistry, health implications, and technological considerations. J Food Sci, 72, 138-51.
  28. Holden JM, Eldridge AL, Beecher GR, et al (1999). Carotenoid Content of U.S. Foods: An Update of the Database. J Food Comp Anal, 12, 169-96. https://doi.org/10.1006/jfca.1999.0827
  29. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans (1991). Volume 51. Coffee, Tea, Mate, methylxanthines and methylglyoxal. IARC, Lyon, France, 273-87.
  30. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans (2010). Volume 92. Some non-heterocyclic polycyclic aromatic hydrocarbons and some related exposures. IARC, Lyon, France, 92, 1-853.
  31. IARC Monographs on the Evaluation of carcinogenic risks to humans (2014). Report of the advisory group to recommend priorities for IARC Monographs during 2015-2019, Lyon.
  32. Jaiswal R, Sovdat T, Vivan F, Kuhnert N (2010). Profiling and characterization by LC-MSn of the chlorogenic acids and hydroxycinnamoylshikimate esters in mate (ilex paraguariensis). J Agricult Food Chem, 58, 5471-84. https://doi.org/10.1021/jf904537z
  33. Jiang W, Wu Y, Jiang X (2013). Coffee and caffeine intake and breast cancer risk: an updated dose-response meta-analysis of 37 published studies. Gynecol Oncol, 129, 620-9. https://doi.org/10.1016/j.ygyno.2013.03.014
  34. Kashyap D, Tuli HS, Sharma AK. (2016) Ursolic acid (UA): A metabolite with promising therapeutic potential. Life Sci, 146, 201-13. https://doi.org/10.1016/j.lfs.2016.01.017
  35. Kassi E, Sourlingas TG, Spiliotaki M, et al (2009). Ursolic acid triggers apoptosis and Bcl-2 downregulation in MCF-7 breast cancer cells. Cancer Invest, 27, 723-33. https://doi.org/10.1080/07357900802672712
  36. Kim HI, Quan FS, Kim JE, et al (2014). Inhibition of estrogen signaling through depletion of estrogen receptor alpha by ursolic acid and betulinic acid from Prunella vulgaris var. lilacina. Biochem Biophys Res Comm, 451, 282-7. https://doi.org/10.1016/j.bbrc.2014.07.115
  37. Lee WJ, Zhu BT (2006). Inhibition of DNA methylation by caffeic acid and chlorogenic acid, two common catecholcontaining coffee polyphenols. Carcinogenesis, 27, 269-77. https://doi.org/10.1093/carcin/bgi206
  38. Li L, Xu LJ, Peng Y, Shi RB, Xiao PG (2011) Comparison of green tea and four other kind of teas. China J Chin Mater Med, 36, 5-10.
  39. Li L, Xu LJ, Ma GZ, et al (2013). The large-leaved Kudingcha (Ilex latifolia Thunb and Ilex kudingcha C.J. Tseng): a traditional Chinese tea with plentiful secondary metabolites and potential biological activities. J Nat Med, 67, 425-37. https://doi.org/10.1007/s11418-013-0758-z
  40. Lima JP, Fara A, King B, et al (2016). Distribution of Major Chlorogenic Acids and Related Compounds in Brazilian Green and Toasted Ilex paraguariensis (Mate) Leaves. J Agric Food Chem, 64, 2361-70. https://doi.org/10.1021/acs.jafc.6b00276
  41. Liu J (1995). Pharmacology of oleanolic acid and ursolic acid. Ethnopharmacol, 49, 57-68. https://doi.org/10.1016/0378-8741(95)90032-2
  42. Mazzei ME, Puchulu MR, Rochaix MA (1995). Table of food chemical composition. Ed. Cenexa y Feiden, Buenos Aires, 2nd ed. (in Spanish)
  43. Newmark HL (1999). Squalene, olive oil, and cancer risk. Review and Hypothesis. In: Cancer Prevention. Novel nutrient and pharmaceutical developments. Ann NY Acad Sci, 889, 193-203. https://doi.org/10.1111/j.1749-6632.1999.tb08735.x
  44. Nie XC, Dong DS, Bai Y, Xia P (2014). Meta-analysis of black tea consumption and breast cancer risk: update 2013. Nutr Cancer, 66, 1009-14. https://doi.org/10.1080/01635581.2014.936947
  45. Noratto G, Porter W, Byrne D, Cisneros-Zevallos L (2009). Identifying peach and plum polyphenols with chemopreventive potential against estrogen-independent breast cancer cells. J Agric Food Chem, 57, 5219-26. https://doi.org/10.1021/jf900259m
  46. Novotny L, Vachalkova A, Biggs D (2001). Ursolic acid: an antitumorigenic and chemopreventive activity. Minireview. Neoplasma, 48, 241-6.
  47. Okoh V, Deoraj A, Roy D (2011). Estrogen-induced reactive oxygen species-mediated signalings contribute to breast cancer. Biochim Biophys Acta, 1815, 115-33.
  48. Price KR, Johnson IT, Fenwick GR (1987). The chemistry and biological significance of saponins in foods and feedingstuffs. CRC Crit Rev Food Sci Nutr, 26, 27-135. https://doi.org/10.1080/10408398709527461
  49. Puangpraphant S, Berhow MA, Gonzalez de Mejia E (2011). Mate (Ilex paraguariensis St. Hilaire) saponins induce caspase-3-dependent apoptosis in human colon cancer cells in vitro. Food Chemistry, 125, 1171-8. https://doi.org/10.1016/j.foodchem.2010.10.023
  50. Puangpraphant S, Dia VP, Gonzalez de Mejia E, et al (2013). Yerba mate tea and mate saponins prevented azoxymethaneinduced inflammation of rat colon through suppression of NF-kB p65ser311 signaling via IkB-a and GSK-3b reduced phosphorylation. Biofactors, 39, 430-40. https://doi.org/10.1002/biof.1083
  51. Ronco AL, De Stefani E, Boffetta P, et al (1999). Vegetables, fruits, and related nutrients and risk of breast cancer: a case control study in Uruguay. Nutr Cancer, 35, 111-9. https://doi.org/10.1207/S15327914NC352_3
  52. Ronco AL, De Stefani E, Boffetta P, et al (2006). Food patterns and risk of breast cancer: A factor analysis study in Uruguay. Int J Cancer, 119, 1672-8. https://doi.org/10.1002/ijc.22021
  53. Ronco AL, De Stefani E, Stoll M (2010a). Hormonal and metabolic modulation through nutrition: towards a primary prevention of breast cancer. Breast, 19, 322-32. https://doi.org/10.1016/j.breast.2010.05.005
  54. Ronco AL, De Stefani E, Aune D, et al (2010b). Nutrient patterns and risk of breast cancer in Uruguay. Asian Pac J Cancer Prev, 11, 519-24.
  55. Ronco AL, De Stefani E (eds) (2012). Nutritional epidemiology of breast cancer. Springer Publishers, Dordrecht.
  56. Ronco AL, De Stefani E, Deneo-Pellegrini H (2012). Risk factors of premenopausal Breast Cancer: A Case-Control Study in Uruguay. Asian Pac J Cancer Prev, 13, 2879-86. https://doi.org/10.7314/APJCP.2012.13.6.2879
  57. Ronco AL, De Stefani E (2013a). Nutrition and breast cancer in pre- and post-menopausal women in Uruguay. In: Collins CJ, Ross Watson R, Preedy VR (eds.) Handbook of Nutrition and Diet in Menopause. Humana Press, New York, 281-92.
  58. Ronco AL, De Stefani E (2013b). Squalene: a multi-task link in the crossroads of cancer and aging. Funct Foods Health Dis, 3, 462-76.
  59. Ronco AL, De Stefani E, Mendoza B, Abbona E, Deneo-Pellegrini H (2016a). Hot infusions and risk of breast cancer: a case-control study in Uruguay. 10th European Breast Cancer Conference, Amsterdam, March 9-11th, 2016, Abst. $N^{\circ}114$. Eur J Cancer, 57, 19-153. https://doi.org/10.1016/S0959-8049(16)31962-1
  60. Ronco AL, De Stefani E, Mendoza B, et al (2016b). Mate intake and risk of breast cancer: a case-control study. Asian Pac J Cancer Prev, 17, 1453-61. https://doi.org/10.7314/APJCP.2016.17.3.1453
  61. Ronco AL, De Stefani E, Mendoza B, et al (2016c). Dietary patterns and risk of breast cancer: a factor analysis of foods and nutrients. Rev Med Uruguay (in press) (in Spanish)
  62. Roy D, Liehr JG (1990). Inhibition of estrogen-induced kidney carcinogenesis in Syrian hamsters by modulators of estrogen metabolism. Carcinogenesis, 11, 567-70. https://doi.org/10.1093/carcin/11.4.567
  63. Roy D, Liehr JG (1999). Estrogen, DNA damage and mutations. Mutat Res, 424, 107-15. https://doi.org/10.1016/S0027-5107(99)00012-3
  64. Roy D, Cai Q, Felty Q, Narayan S (2007). Estrogen-induced generation of reactive oxygen and nitrogen species, gene damage, and estrogen-dependent cancers. J Toxicol Environ Health B Crit Rev, 10, 235-57. https://doi.org/10.1080/15287390600974924
  65. Roy D, Singh KP (2004). Estrogen-induced genetic alterations and their role in carcinogenicity. Current Genomics, 5, 245-57. https://doi.org/10.2174/1389202043349471
  66. Satoh K, Sakamoto Y, Ogata A, et al (2002). Inhibition of aromatase activity by green tea extract catechins and their endocrinological effects of oral administration in rats. Food Chem Toxicol, 40, 925-33. https://doi.org/10.1016/S0278-6915(02)00066-2
  67. Shishodia S, Majumdar S, Banerjee S, Aggarwal BB (2003). Ursolic acid inhibits nuclear factor-${\kappa}B$ activation induced by carcinogenic agents through suppression of $I{\kappa}B{\alpha}$ kinase and p65 phosphorylation correlation with down-regulation of cyclooxygenase2, Matrix Metalloproteinase 9, and Cyclin D1. Cancer Res, 63, 4375-83.
  68. Souza AHP, Correa RCG, Barros L, et al (2015). Phytochemicals and bioactive properties of Ilex paraguariensis: An in-vitro comparative study between the whole plant, leaves and stems. Food Res Int, 78, 286-94. https://doi.org/10.1016/j.foodres.2015.09.032
  69. Subbaramaiah K, Michaluart P, Sporn MB, Dannenberg AJ (2000). Ursolic acid inhibits cyclooxygenase-2 transcription in human mammary epithelial cells. Cancer Res, 60, 2399-404.
  70. Szaefer H, Krajka-Kuzniak V, Ignatowicz E, et al (2014). The effect of cloudy apple juice on hepatic and mammary gland phase I and II enzymes induced by DMBA in female Sprague-Dawley rats. Drug Chem Toxicol, 37, 472-9. https://doi.org/10.3109/01480545.2014.893442
  71. Tan KW, Li Y, Paxton JW, Birch NP, Scheepens A (2013). Identification of novel dietary phytochemicals inhibiting the efflux transporter breast cancer resistance protein (BCRP/ABCG2). Food Chem, 138, 2267-74. https://doi.org/10.1016/j.foodchem.2012.12.021
  72. Thea AE, Ferreira D, Brumovsky LA, Schmalko ME (2016). Polycyclic aromatic hydrocarbons (PAHs) in yerba mate (Ilex paraguariensis St. Hil) traditional infusions (mate and terere). Food Control, 60, 215-20. https://doi.org/10.1016/j.foodcont.2015.07.046
  73. Tiwari P, Sahay S, Pandey M, et al (2014). Combinatorial chemopreventive effect of butyric acid, nicotinamide and calcium glucarate against the 7,12-dimethylbenz(a) anthracene induced mouse skin tumorigenesis attained by enhancing the induction of intrinsic apoptotic events. Chem Biol Interact, 226, 1-11.
  74. Wang J, Ren T, Xi T (2012). Ursolic acid induces apoptosis by suppressing the expression of FoxM1 in MCF-7 human breast cancer cells. Med Oncol, 29, 10-5. https://doi.org/10.1007/s12032-010-9777-8
  75. Wang J, Tang L, Wang JS (2015). Biomarkers of Dietary Polyphenols in Cancer Studies: Current Evidence and Beyond. Oxid Med Cell Longevity.
  76. Way TD, Lee HH, Kao MC, Lin JK (2004). Black tea polyphenol theaflavins inhibit aromatase activity and attenuate tamoxifen resistance in HER2/neu-transfected human breast cancer cells through tyrosine kinase suppression. Eur J Cancer, 40, 2165-74. https://doi.org/10.1016/j.ejca.2004.06.018
  77. Wierzbicka GT, Hagen TM, Jones DP (1989). Glutathione in food. J Food Comp Anal, 2, 327-37. https://doi.org/10.1016/0889-1575(89)90004-5
  78. Wu Y, Zhang D, Kang S (2013). Black tea, green tea and risk of breast cancer: an update. Springer Plus, 2, 240. https://doi.org/10.1186/2193-1801-2-240
  79. Yeh CT, Wu CH, Yen GC (2010). Ursolic acid, a naturally occurring triterpenoid, suppresses migration and invasion of human breast cancer cells by modulating c-Jun N-terminal kinase, Akt and mammalian target of rapamycin signalling. Mol Nutr Food Res, 54, 1285-95. https://doi.org/10.1002/mnfr.200900414
  80. Yogeeswari P, Sriram D (2005). Betulinic acid and its derivatives: a review on their biological properties. Curr Med Chem, 12, 657-66. https://doi.org/10.2174/0929867053202214
  81. Yoon H, Liu RH (2007). Effect of selected phytochemicals and apple extracts on NF-kB activation in human breast cancer MCF-7 cells. J Agric Food Chem, 55, 3167-73. https://doi.org/10.1021/jf0632379