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Soy and tea intake on cervical cancer risk: the Singapore Chinese Health Study

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Abstract

Purpose

Soy isoflavones and tea catechins have immunomodulating and chemopreventive properties relevant for cervical carcinogenesis; however, there are limited epidemiologic data on the relationship of soy and tea consumption with cervical cancer risk. The aim of our study was to examine effects of soy and tea intake on cervical cancer risk among Singapore Chinese women.

Methods

The association between intake of soy and tea drinking and cervical cancer risk was investigated in a prospective, population-based cohort of 30,744 Chinese women in Singapore with an average 16.7 years of follow-up and 312 incident cervical cancer cases. Multivariable proportional hazard models were used to estimate hazard ratio (HR) and 95% confidence interval (CI) of cervical cancer associated with intake levels of soy and tea.

Results

High intake of soy alone was associated with a statistically borderline significant 20% reduced risk of cervical cancer (HR 0.80, 95% CI 0.61, 1.05) while green tea alone was not (HR 0.97, 95% CI: 0.76, 1.22). In stratified analysis, high intake of soy was associated with a statistically significant decrease in cervical cancer risk among green tea drinkers (HR 0.43; 95% CI 0.28, 0.69) but not among non-drinkers of green tea. The difference in the soy-cervical cancer risk association between green tea drinkers and non-drinkers was statistically significant (p for interaction = 0.004). This inverse association between soy intake and cervical cancer risk remained after further adjustment for human papillomavirus serostatus. Black tea consumption was not associated with cervical cancer risk.

Conclusions

These findings suggest that a protective effect of soy against cervical cancer development may depend on green tea constituents.

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Abbreviations

BMI:

Body mass index

CI:

Confidence interval

CIS:

Carcinoma in situ

EGCG:

Epigallocatechin-3-gallate

HR:

Hazard ratio

HPV:

Human papillomavirus

HSV-2:

Herpes simplex virus 2

OC:

Oral contraceptive

OR:

Odds ratio

References

  1. Vaccarella S, Lortet-Tieulent J, Plummer M et al (2013) Worldwide trends in cervical cancer incidence: impact of screening against changes in disease risk factors. Eur J Cancer 49:3262–3273. https://doi.org/10.1016/j.ejca.2013.04.024

    Article  PubMed  Google Scholar 

  2. Schiffman M, Castle PE, Jeronimo J et al (2007) Human papillomavirus and cervical cancer. Lancet 370:890–907. https://doi.org/10.1016/S0140-6736(07)61416-0

    Article  CAS  PubMed  Google Scholar 

  3. Laara E, Day NE, Hakama M (1987) Trends in mortality from cervical cancer in the Nordic countries: association with organised screening programmes. Lancet 1:1247–1249

    Article  CAS  PubMed  Google Scholar 

  4. Gakidou E, Nordhagen S, Obermeyer Z (2008) Coverage of cervical cancer screening in 57 countries: low average levels and large inequalities. PLoS Med 5:0863–0868. https://doi.org/10.1371/journal.pmed.0050132

    Article  Google Scholar 

  5. Newmann SJ, Garner EO (2005) Social inequities along the cervical cancer continuum: a structured review. Cancer Causes Control 16:63–70. https://doi.org/10.1007/s10552-004-1290-y

    Article  PubMed  Google Scholar 

  6. Bruni L, Barrionuevo-Rosas L, Albero G, et al (2015) Human papillomavirus and related diseases in the world. Summary Report 2015-04-08

  7. Castellsagué X (2008) Natural history and epidemiology of HPV infection and cervical cancer. Gynecol Oncol 110:S4–S7. https://doi.org/10.1016/j.ygyno.2008.07.045

    Article  PubMed  Google Scholar 

  8. Castellsague X, Munoz N (2003) Chapter 3: cofactors in human papillomavirus carcinogenesis–role of parity, oral contraceptives, and tobacco smoking. JNCI Monogr https://doi.org/10.1093/oxfordjournals.jncimonographs.a003477

  9. Delvenne P, Herman L, Kholod N et al (2007) Role of hormone cofactors in the human papillomavirus-induced carcinogenesis of the uterine cervix. Mol Cell Endocrinol 264:1–5. https://doi.org/10.1016/j.mce.2006.10.014

    Article  CAS  PubMed  Google Scholar 

  10. Wu AH, Yu MC, Tseng C-C, Pike MC (2008) Epidemiology of soy exposures and breast cancer risk. Br J Cancer 98:9–14. https://doi.org/10.1038/sj.bjc.6604145

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Yan L, Spitznagel EL (2009) Soy consumption and prostate cancer risk in men: a revisit of a meta-analysis. Am J Clin Nutr 89:1155–1163. https://doi.org/10.3945/ajcn.2008.27029

    Article  CAS  PubMed  Google Scholar 

  12. Ko K-P, Park SK, Yang JJ et al (2013) Intake of soy products and other foods and gastric cancer risk: a prospective study. J Epidemiol 23:337–343

    Article  PubMed  PubMed Central  Google Scholar 

  13. Wu SH, Liu Z (2013) Soy food consumption and lung cancer risk: a meta-analysis using a common measure across studies. Nutr Cancer 65:625–632. https://doi.org/10.1080/01635581.2013.795983

    Article  CAS  PubMed  Google Scholar 

  14. Roy M, Siddiqi M, Bhattacharya RK (2001) MINI-REVIEW Cancer Chemoprevention: tea polyphenol induced cellular and molecular responses. Asian Pac J Cancer Prev 2:109–116

    PubMed  Google Scholar 

  15. Butler LM, Wu AH (2011) Green and black tea in relation to gynecologic cancers. Mol Nutr Food Res 55:931–940. https://doi.org/10.1002/mnfr.201100058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Wang Y, Ho C-T (2009) Polyphenolic chemistry of tea and coffee: a century of progress. J Agric Food Chem 57:8109–8114. https://doi.org/10.1021/jf804025c

    Article  CAS  PubMed  Google Scholar 

  17. Wang ZY, Huang M, Lou Y, Reuhi R (1994) Inhibitory effects of black tea, green tea, decaffeinated black tea, and decaffeinated green tea on ultraviolet B light-induced skin carcinogenesis in 7, 12-dimethylbenz[a]anthracene-initiated SKH-1 mice inhibitory effects of black tea, green tea. Cancer Res 54:3425–3428

    Google Scholar 

  18. Yuan J-M, Stram DO, Arakawa K et al (2003) Dietary cryptoxanthin and reduced risk of lung cancer: the Singapore Chinese Health Study. Cancer Epidemiol Biomarkers Prev 12:890–898

    CAS  PubMed  Google Scholar 

  19. Hankin JH, Stram DO, Arakawa K et al (2001) Singapore Chinese Health Study: development, validation, and calibration of the quantitative food frequency questionnaire. Nutr Cancer 39:187–195. https://doi.org/10.1207/S15327914nc392_5

    Article  CAS  PubMed  Google Scholar 

  20. Wu AH, Koh W-P, Wang R et al (2008) Soy intake and breast cancer risk in Singapore Chinese Health Study. Br J Cancer 99:196–200. https://doi.org/10.1038/sj.bjc.6604448

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Wu AH, Stanczyk FZ, Seow A et al (2002) Soy intake and other lifestyle determinants of serum estrogen levels among postmenopausal Chinese women in Singapore. Cancer Epidemiol Biomark Prev 11:844–851

    CAS  Google Scholar 

  22. Seow A, Shi CY, Franke AA et al (1998) Isoflavonoid levels in spot urine are associated with frequency of dietary soy intake in a population-based sample of middle-aged and older Chinese in Singapore. Cancer Epidemiol Biomark Prev 7:135–140

    CAS  Google Scholar 

  23. Yuan J-M, Gao Y-T, Yang CS, Yu MC (2007) Urinary biomarkers of tea polyphenols and risk of colorectal cancer in the Shanghai Cohort Study. Int J Cancer 120:1344–1350. https://doi.org/10.1002/ijc.22460

    Article  CAS  PubMed  Google Scholar 

  24. Parkin DM (2006) The global health burden of infection-associated cancers in the year 2002. Int J Cancer 118:3030–3044. https://doi.org/10.1002/ijc.21731

    Article  CAS  PubMed  Google Scholar 

  25. Waterboer T, Sehr P, Michael KM et al (2005) Multiplex human papillomavirus serology based on in situ-purified glutathione s-transferase fusion proteins. Clin Chem 51:1845–1853. https://doi.org/10.1373/clinchem.2005.052381

    Article  CAS  PubMed  Google Scholar 

  26. Clifford GM, Shin H-R, Oh JK et al (2007) Serologic response to oncogenic human papillomavirus types in male and female university students. Cancer Epidem Biomark Prev 16:1874–1879

    Article  CAS  Google Scholar 

  27. Bosch FX, Lorincz A, Muñoz N et al (2002) The causal relation between human papillomavirus and cervical cancer. J Clin Pathol 55:244–265. https://doi.org/10.1136/jcp.55.4.244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Chih HJ, Lee AH, Colville L et al (2013) A review of dietary prevention of human papillomavirus-related infection of the cervix and cervical intraepithelial neoplasia. Nutr Cancer 65:317–328. https://doi.org/10.1080/01635581.2013.757630

    Article  CAS  PubMed  Google Scholar 

  29. Moore MA, Tajima K, Anh PH et al (2003) Grand challenges in global health and the practical prevention program? Asian focus on cancer prevention in females of the developing world. Asian Pac J Cancer Prev 4:153–165

    PubMed  Google Scholar 

  30. Dhandayuthapani S, Marimuthu P, Hoermann V et al (2013) Induction of apoptosis in HeLa Cells via caspase activation by resveratrol and genistein. J Med Food 16:139–146. https://doi.org/10.1089/jmf.2012.0141

    Article  CAS  PubMed  Google Scholar 

  31. Hussain A, Harish G, Prabhu SA et al (2012) Inhibitory effect of genistein on the invasive potential of human cervical cancer cells via modulation of matrix metalloproteinase-9 and tissue inhibitiors of matrix metalloproteinase-1 expression. Cancer Epidemiol 36:e387–e393. https://doi.org/10.1016/j.canep.2012.07.005

    Article  CAS  PubMed  Google Scholar 

  32. Kim S-H, Kim S-H, Lee S-C, Song Y-S (2009) Involvement of both extrinsic and intrinsic apoptotic pathways in apoptosis induced by genistein in human cervical cancer cells. Ann N Y Acad Sci 1171:196–201. https://doi.org/10.1111/j.1749-6632.2009.04902.x

    Article  CAS  PubMed  Google Scholar 

  33. Xiao JX, Huang GQ, Geng X, Qiu HW (2011) Soy-derived isoflavones inhibit HeLa Cell growth by Inducing apoptosis. Plant Foods Hum Nutr 66:122–128. https://doi.org/10.1007/s11130-011-0224-6

    Article  CAS  PubMed  Google Scholar 

  34. Chung S, Franceschi S, Lambert P (2010) Estrogen and ERα: culprits in cervical cancer? Trends Endocrinol 21:504–511. https://doi.org/10.1016/j.tem.2010.03.005.estrogen

  35. Brake T, Lambert PF (2005) Estrogen contributes to the onset, persistence, and malignant progression of cervical cancer in a human papillomavirus-transgenic mouse model. Proc Natl Acad Sci U S A 102:2490–2495. https://doi.org/10.1073/pnas.0409883102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Kim J (2008) Protective effects of Asian dietary items on cancers—soy and ginseng. Asian Pac J Cancer Prev 9:543–548

    PubMed  Google Scholar 

  37. Miller PE, Snyder DC (2012) Phytochemicals and cancer risk: a review of the epidemiological evidence. Nutr Clin Pract 27:599–612. https://doi.org/10.1177/0884533612456043

    Article  PubMed  Google Scholar 

  38. Fuhrman BJ, Pfeiffer RM, Wu AH et al (2013) Green tea intake is associated with urinary estrogen profiles in Japanese-American women. Nutr J 12:25. https://doi.org/10.1186/1475-2891-12-25

    Article  PubMed  PubMed Central  Google Scholar 

  39. Wu AH, Arakawa K, Stanczyk FZ et al (2005) Tea and circulating estrogen levels in postmenopausal Chinese women in Singapore. Carcinogenesis 26:976–980. https://doi.org/10.1093/carcin/bgi028

    Article  CAS  PubMed  Google Scholar 

  40. Wu AH, Yu MC (2006) Tea, hormone-related cancers and endogenous hormone levels. Mol Nutr Food Res 50:160–169. https://doi.org/10.1002/mnfr.200500142

    Article  CAS  PubMed  Google Scholar 

  41. Hsu A, Bruno RS, Löhr CV et al (2012) Dietary soy and tea mitigate chronic inflammation and prostate cancer via NFκB pathway in the Noble rat model. J Nutr Biochem 22:502–510. https://doi.org/10.1016/j.jnutbio.2010.04.006.Dietary

    Article  Google Scholar 

  42. Nair S, Pillai MR (2005) Human papillomavirus and disease mechanisms: relevance to oral and cervical cancers. Oral Dis 11:350–359. https://doi.org/10.1111/j.1601-0825.2005.01127.x

    Article  CAS  PubMed  Google Scholar 

  43. Baeza I, De la Fuente M (2013) The role polyphenols in menopause. In: Nutition and diet in menopause. pp 51–63

  44. Jin L, Qi M, Chen DZ et al (1999) Indole-3-carbinol prevents cervical cancer in human papilloma virus type 16 (HPV16) transgenic mice. Cancer Res 59:3991–3997

    CAS  PubMed  Google Scholar 

  45. Jia Y, Hu T, Hang C-Y et al (2012) Case–control study of diet in patients with cervical cancer or precancerosis in Wufeng, a high incidence region in China. Asian Pac J Cancer Prev 13:5299–5302. https://doi.org/10.7314/APJCP.2012.13.10.5299

    Article  PubMed  Google Scholar 

  46. Hernandez BY, McDuffie K, Franke AA et al (2004) Reports: plasma and dietary phytoestrogens and risk of premalignant lesions of the cervix. Nutr Cancer 49:109–124. https://doi.org/10.1207/s15327914nc4902_1

    Article  CAS  PubMed  Google Scholar 

  47. Guo JM, Kang GZ, Xiao BX et al (2004) Effect of daidzein on cell growth, cell cycle, and telomerase activity of human cervical cancer in vitro. Int J Gynecol Cancer 14:882–888. https://doi.org/10.1111/j.1048-891X.2004.14525.x

    Article  CAS  PubMed  Google Scholar 

  48. Kim EY, Shin JY, Park Y, Kim AK (2014) Equol Induces Mitochondria-mediated Apoptosis of Human Cervical Cancer Cells. Anticancer Res 34:4985–4992

    CAS  PubMed  Google Scholar 

  49. Zhang Y-F, Xu Q, Lu J et al (2014) Tea consumption and the incidence of cancer: a systematic review and meta-analysis of prospective observational studies. Eur J Cancer Prev 1:10. https://doi.org/10.1097/cej.0000000000000094

    Article  Google Scholar 

  50. Montague JA, Butler LM, Wu AH et al (2012) Green and black tea intake in relation to prostate cancer risk among Singapore Chinese. Cancer Causes Control 23:1635–1641. https://doi.org/10.1007/s10552-012-0041-8

    Article  PubMed  PubMed Central  Google Scholar 

  51. Stanley M, Pinto LA, Trimble C (2012) Human papillomavirus vaccines—immune responses. Vaccine 30:F83–F87. https://doi.org/10.1016/j.vaccine.2012.04.106

    Article  CAS  PubMed  Google Scholar 

  52. Tiggelaar SM, Lin MJ, Viscidi RP et al (2012) Age-specific human papillomavirus antibody and deoxyribonucleic acid prevalence: a global review. J Adolesc Heal 50:110–131. https://doi.org/10.1016/j.jadohealth.2011.10.010

    Article  Google Scholar 

  53. Keinan-Boker L, Peeters P, Mulligan A et al (2002) Soy product consumption in 10 European countries: the European Prospective Investigation into Cancer and Nutrition (EPIC) study. Public Health Nutr 5:1217. https://doi.org/10.1079/PHN2002400

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Siew-Hong Low of the National University of Singapore for supervising the fieldwork of the Singapore Chinese Health Study, and the Singapore Cancer Registry for assistance with the identification of cancer outcomes.

Funding

This work was supported by the United States National Cancer Institute at the National Institutes of Health (UM1 CA182876 and R01 CA144034). WPK was supported by the National Medical Research Council, Singapore (NMRC/CSA/0055/2013).

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Authors and Affiliations

  1. Department of Epidemiology, Graduate School of Public Health, University of Pittsburgh, 130 De Soto St, Pittsburgh, PA, 15261, USA

    Proma Paul, Jian-Min Yuan & Lesley M. Butler

  2. Health Services and Systems Research, Duke-NUS Medical School, Singapore, Singapore

    Woon-Puay Koh & Aizhen Jin

  3. Saw Swee Hock School of Public Health, National University of Singapore, Singapore, Singapore

    Woon-Puay Koh

  4. Division of Molecular Diagnostics of Oncogenic Infections, German Cancer Research Center (DKFZ), Heidelberg, Germany

    Angelika Michel, Tim Waterboer & Michael Pawlita

  5. Cancer Control and Population Sciences, University of Pittsburgh Cancer Institute, Pittsburgh, PA, USA

    Renwei Wang, Jian-Min Yuan & Lesley M. Butler

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  1. Proma Paul
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Correspondence to Proma Paul.

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Paul, P., Koh, WP., Jin, A. et al. Soy and tea intake on cervical cancer risk: the Singapore Chinese Health Study. Cancer Causes Control 30, 847–857 (2019). https://doi.org/10.1007/s10552-019-01173-3

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