Phyto-oestrogens and colorectal cancer risk: A systematic review and dose-response meta-Analysis of observational studies

British Journal of Nutrition

Volumn 116, Issue 12, 2016, Pages 2115-2128

  Jiang, Ruijingfang ^a   Botma, Akke ^a   Rudolph, Anja ^a   Hüsing, Anika ^a   Chang Claude, Jenny ^a,b  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

Colorectal cancer; Isoflavones; Lignans; Meta Analyses; Phyto oestrogens

Indexed keywords

ENTEROLACTONE; ISOFLAVONE DERIVATIVE; LIGNAN; PHYTOESTROGEN;

ASIAN; CANCER RISK; CASE CONTROL STUDY; COHORT ANALYSIS; COLORECTAL CANCER; CONCENTRATION RESPONSE; FOOD FREQUENCY QUESTIONNAIRE; FOOD INTAKE; HUMAN; LIQUID CHROMATOGRAPHY-MASS SPECTROMETRY; OBSERVATIONAL STUDY; QUANTITATIVE ANALYSIS; REVIEW; RISK ASSESSMENT; RISK REDUCTION; SYSTEMATIC REVIEW; ADENOMA; ANIMAL; COLORECTAL NEOPLASMS; COMPARATIVE STUDY; EVIDENCE BASED MEDICINE; FEMALE; FUNCTIONAL FOOD; HEALTHY DIET; INCIDENCE; MALE; META ANALYSIS; REPRODUCIBILITY; RISK; SEX DIFFERENCE; SOY FOOD;

ADENOMA; ANIMALS; COLORECTAL NEOPLASMS; EVIDENCE-BASED MEDICINE; FEMALE; FUNCTIONAL FOOD; HEALTHY DIET; HUMANS; INCIDENCE; ISOFLAVONES; LIGNANS; MALE; OBSERVATIONAL STUDIES AS TOPIC; PHYTOESTROGENS; REPRODUCIBILITY OF RESULTS; RISK; SEX FACTORS; SOY FOODS;

EID: 85009827322     PISSN: 00071145     EISSN: 14752662     Source Type: Journal    
DOI: 10.1017/S0007114516004360     Document Type: Review

References (63)

1. Ferlay JSI, Ervik M, Dikshit R, et al. (2013) Cancer incidence and mortality worldwide: IARC CancerBase no. 11. http://globocan.iarc.fr (accessed January 2016).
2. Pampaloni CMB, Bartolini E, Tonelli F, et al. (2013) Phytoestrogens and colon cancer. In Soybean-Bio-Active Compounds, pp. 75-96 [HA El-Shemy, editor]. InTech.
3. Kuiper GG, Carlsson B, Grandien K, et al. (1997) Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 138, 863-870.
4. Kuiper GG, Lemmen JG, Carlsson B, et al. (1998) Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 139, 4252-4263.
5. Barzi A, Lenz AM, Labonte MJ, et al. (2013) Molecular pathways: estrogen pathway in colorectal cancer. Clin Cancer Res 19, 5842-5848.
6. Cornwell T, Cohick W & Raskin I (2004) Dietary phytoestrogens and health. Phytochemistry 65, 995-1016.
7. Thompson LU, Boucher BA, Liu Z, et al. (2006) Phytoestrogen content of foods consumed in Canada, including isoflavones, lignans, and coumestan. Nutr Cancer 54, 184-201.
8. Kuhnle GG, DellAquila C, Aspinall SM, et al. (2008) Phytoestrogen content of foods of animal origin: dairy products, eggs, meat, fish, and seafood. J Agric Food Chem 56, 10099-10104.
9. Zamora-Ros R, Knaze V, Lujan-Barroso L, et al. (2012) Dietary intakes and food sources of phytoestrogens in the European Prospective Investigation into Cancer and Nutrition (EPIC) 24-hour dietary recall cohort. Eur J Clin Nutr 66, 932-941.
10. Valentin-Blasini L, Sadowski MA, Walden D, et al. (2005) Urinary phytoestrogen concentrations in the U.S. population (1999-2000). J Expo Anal Environ Epidemiol 15, 509-523.
11. Rowland I, Faughnan M, Hoey L, et al. (2003) Bioavailability of phyto-oestrogens. Br J Nutr 89, Suppl. 1, S45-S58.
12. Zubik L & Meydani M (2003) Bioavailability of soybean isoflavones from aglycone and glucoside forms in American women. Am J Clin Nutr 77, 1459-1465.
13. Yan L, Spitznagel EL & Bosland MC (2010) Soy consumption and colorectal cancer risk in humans: A meta-Analysis. Cancer Epidemiol Biomarkers Prev 19, 148-158.
14. Woo HD & Kim J (2013) Dietary flavonoid intake and risk of stomach and colorectal cancer. World J Gastroenterol 19, 1011-1019.
15. Akhter M, Iwasaki M, Yamaji T, et al. (2009) Dietary isoflavone and the risk of colorectal adenoma: A case-control study in Japan. Br J Cancer 100, 1812-1816.
16. Cotterchio M, Boucher BA, Manno M, et al. (2006) Dietary phytoestrogen intake is associated with reduced colorectal cancer risk. J Nutr 136, 3046-3053.
17. Ravasco P, Monteiro-Grillo I, Marques Vidal P, et al. (2005) Nutritional risks and colorectal cancer in a Portuguese population. Nutr Hosp 20, 165-172.
18. Rossi M, Negri E, Talamini R, et al. (2006) Flavonoids and colorectal cancer in Italy. Cancer Epidemiol Biomarkers Prev 15, 1555-1558.
19. Shin A, Lee J, Lee J, et al. (2015) Isoflavone and soyfood intake and colorectal cancer risk: A case-control study in Korea. PLOS ONE 10, e0143228.
20. Zamora-Ros R, Not C, Guinó E, et al. (2013) Association between habitual dietary flavonoid and lignan intake and colorectal cancer in a Spanish case-control study (the Bellvitge Colorectal Cancer Study). Cancer Causes Control 24, 549-557.
21. Yang G, Shu XO, Li H, et al. (2009) Prospective cohort study of soy food intake and colorectal cancer risk in women. Am J Clin Nutr 89, 577-583.
22. Ward HA, Kuhnle GGC, Mulligan AA, et al. (2010) Breast, colorectal, and prostate cancer risk in the European Prospective Investigation into Cancer and Nutrition-Norfolk in relation to phytoestrogen intake derived from an improved database. Am J Clin Nutr 91, 440-448.
23. Oba S, Nagata C, Shimizu N, et al. (2007) Soy product consumption and the risk of colon cancer: A prospective study in Takayama, Japan. Nutr Cancer 57, 151-157.
24. Butler LM, Wang R, Koh WP, et al. (2008) Prospective study of dietary patterns and colorectal cancer among Singapore Chinese. Br J Cancer 99, 1511-1516.
25. Budhathoki S, Joshi AM, Ohnaka K, et al. (2011) Soy food and isoflavone intake and colorectal cancer risk: The Fukuoka Colorectal Cancer Study. Scand J Gastroenterol 46, 165-172.
26. Akhter M, Inoue M, Kurahashi N, et al. (2008) Dietary soy and isoflavone intake and risk of colorectal cancer in the Japan public health center-based prospective study. Cancer Epidemiol Biomarkers Prev 17, 2128-2135.
27. Ward H, Chapelais G, Kuhnle GGC, et al. (2008) Lack of prospective associations between plasma and urinary phytoestrogens and risk of prostate or colorectal cancer in the European Prospective into Cancer-Norfolk study. Cancer Epidemiol Biomarkers Prev 17, 2891-2894.
28. Hedelin M, Lof M, Sandin S, et al. (2016) Prospective study of dietary phytoestrogen intake and the risk of colorectal cancer. Nutr Cancer 68, 388-395.
29. Tse G & Eslick GD (2016) Soy and isoflavone consumption and risk of gastrointestinal cancer: A systematic review and meta-Analysis. Eur J Nutr 55, 63-73.
30. Moher D, Liberati A, Tetzlaff J, et al. (2009) Preferred reporting items for systematic reviews and meta-Analyses: The PRISMA statement. PLoS Med 6, e1000097.
31. Wells GA, Shea B, OConnell D, Peterson J, et al. (2000) The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-Analyses. http://www.ohri. ca/programs/clinical-epidemiology/oxford.asp (accessed January 2016).
32. Greenland S & Longnecker MP (1992) Methods for trend estimation from summarized dose-response data, with applications to meta-Analysis. Am J Epidemiol 135, 1301-1309.
33. Orsini N, Li R, Wolk A, et al. (2012) Meta-Analysis for linear and nonlinear dose-response relations: examples, an evaluation of approximations, and software. Am J Epidemiol 175, 66-73.
34. Harrell FE Jr., Lee KL & Pollock BG (1988) Regression models in clinical studies: determining relationships between predictors and response. J Natl Cancer Inst 80, 1198-1202.
35. Kuijsten A, Arts ICW, Hollman PCH, et al. (2006) Plasma enterolignans are associated with lower colorectal adenoma risk. Cancer Epidemiol Biomarkers Prev 15, 1132-1136.
36. Kuijsten A, Hollman PCH, Boshuizen HC, et al. (2008) Plasma enterolignan concentrations and colorectal cancer risk in a nested case-control study. Am J Epidemiol 167, 734-742.
37. Higgins JP & Thompson SG (2002) Quantifying heterogeneity in a meta-Analysis. Stat Med 21, 1539-1558.
38. Hedges LV & Pigott TD (2001) The power of statistical tests in meta-Analysis. Psychol Methods 6, 203-217.
39. Egger M, Davey Smith G, Schneider M, et al. (1997) Bias in meta-Analysis detected by a simple, graphical test. BMJ 315, 629-634.
40. Viechtbauer W (2010) Conducting meta-Analyses in R with the metafor package. J Stat Softw 36, 1-48.
41. Crippa A & Orsini N (2016) Multivariate dose-response metaanalysis: The dosresmeta R package. J Stat Softw 72, 1-15.
42. Cutler GJ, Nettleton JA, Ross JA, et al. (2008) Dietary flavonoid intake and risk of cancer in postmenopausal women: The Iowa Womens Health Study. Int J Cancer 123, 664-671.
43. Honma N, Yamamoto K, Ohnaka K, et al. (2013) Estrogen receptor-beta gene polymorphism and colorectal cancer risk: effect modified by body mass index and isoflavone intake. Int J Cancer 132, 951-958.
44. Johnsen NF, Olsen A, Thomsen BL, et al. (2010) Plasma enterolactone and risk of colon and rectal cancer in a casecohort study of Danish men and women. Cancer Causes Control 21, 153-162.
45. Li L, Zhang M & Holman CD (2013) Population versus hospital controls in the assessment of dietary intake of isoflavone for case-control studies on cancers in China. Nutr Cancer 65, 390-397.
46. Rossi M, Bosetti C, Negri E, et al. (2010) Flavonoids, proanthocyanidins, and cancer risk: A network of case-control studies from Italy. Nutr Cancer 62, 871-877.
47. Theodoratou E, Kyle J, Cetnarskyj R, et al. (2007) Dietary flavonoids and the risk of colorectal cancer. Cancer Epidemiol Biomarkers Prev 16, 684-693.
48. Butler LM, Koh WP, Wang R, et al. (2010) Soy increases risk of rectal cancer among Singapore Chinese women. Cancer Res 70, 8 Suppl., Abstract 2815.
49. Milder IEJ, Kuijsten A, Arts ICW, et al. (2007) Relation between plasma enterodiol and enterolactone and dietary intake of lignans in a Dutch endoscopy-based population. J Nutr 137, 1266-1271.
50. Kilkkinen A, Stumpf K, Pietinen P, et al. (2001) Determinants of serum enterolactone concentration. Am J Clin Nutr 73, 1094-1100.
51. Horner NK, Kristal AR, Prunty J, et al. (2002) Dietary determinants of plasma enterolactone. Cancer Epidemiol Biomarkers Prev 11, 121-126.
52. Bobe G, Sansbury LB, Albert PS, et al. (2008) Dietary flavonoids and colorectal adenoma recurrence in the Polyp Prevention Trial. Cancer Epidemiol Biomarkers Prev 17, 1344-1353.
53. Bobe G, Murphy G, Albert PS, et al. (2012) Dietary lignan and proanthocyanidin consumption and colorectal adenoma recurrence in the Polyp Prevention Trial. Int J Cancer 130, 1649-1659.
54. Danbara N, Yuri T, Tsujita-Kyutoku M, et al. (2005) Enterolactone induces apoptosis and inhibits growth of Colo 201 human colon cancer cells both in vitro and in vivo. Anticancer Res 25, 2269-2276.
55. Zhang Y, Li Q, Zhou D, et al. (2013) Genistein, a soya isoflavone, prevents azoxymethane-induced up-regulation of WNT/beta-catenin signalling and reduces colon pre-neoplasia in rats. Br J Nutr 109, 33-42.
56. Thiagarajan DG, Bennink MR, Bourquin LD, et al. (1998) Prevention of precancerous colonic lesions in rats by soy flakes, soy flour, genistein, and calcium. Am J Clin Nutr 68, 1394s-1399s.
57. Javid SH, Moran AE, Carothers AM, et al. (2005) Modulation of tumor formation and intestinal cell migration by estrogens in the Apc(Min/+) mouse model of colorectal cancer. Carcinogenesis 26, 587-595.
58. Caiazza F, Ryan EJ, Doherty G, et al. (2015) Estrogen receptors and their implications in colorectal carcinogenesis. Front Oncol 5, 19.
59. Totta P, Acconcia F, Virgili F, et al. (2005) Daidzein-sulfate metabolites affect transcriptional and antiproliferative activities of estrogen receptor-beta in cultured human cancer cells. J Nutr 135, 2687-2693.
60. Principi M, Di Leo A, Pricci M, et al. (2013) Phytoestrogens/insoluble fibers and colonic estrogen receptor beta: randomized, double-blind, placebo-controlled study. World J Gastroenterol 19, 4325-4333.
61. Raju J, Bielecki A, Caldwell D, et al. (2009) Soy isoflavones modulate azoxymethane-induced rat colon carcinogenesis exposed pre-And postnatally and inhibit growth of DLD-1 human colon adenocarcinoma cells by increasing the expression of estrogen receptor-beta. J Nutr 139, 474-481.
62. Barone M, Tanzi S, Lofano K, et al. (2010) Dietary-induced ERbeta upregulation counteracts intestinal neoplasia development in intact male ApcMin/+ mice. Carcinogenesis 31, 269-274.
63. Hartman J, Edvardsson K, Lindberg K, et al. (2009) Tumor repressive functions of estrogen receptor beta in SW480 colon cancer cells. Cancer Res 69, 6100-6106.