Effects of tomato- and soy-rich diets on the IGF-I hormonal network: A crossover study of postmenopausal women at high risk for breast cancer

Cancer Prevention Research

Volumn 4, Issue 5, 2011, Pages 702-710

  McLaughlin, John M ^a,b   Olivo Marston, Susan ^a,b   Vitolins, Mara Z ^d   Bittoni, Marisa ^b   Reeves, Katherine W ^b   Degraffinreid, Cecilia R ^a,b   Schwartz, Steven J ^a,b   Clinton, Steven K ^a,c   Paskett, Electra D ^a,b  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^d WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CAROTENE; C PEPTIDE; CAROTENOID; DAIDZEIN; ESTRADIOL; GENISTEIN; INSULIN; ISOFLAVONE; LYCOPENE; SEX HORMONE BINDING GLOBULIN; SOMATOMEDIN BINDING PROTEIN 3; SOMATOMEDIN C; SOYBEAN PROTEIN;

ADULT; AGED; ARTICLE; BREAST CANCER; CANCER GROWTH; CANCER PREVENTION; CANCER RISK; CONTROLLED STUDY; CROSSOVER PROCEDURE; DIET SUPPLEMENTATION; ESTRADIOL BLOOD LEVEL; FEMALE; FRUIT JUICE; HIGH RISK PATIENT; HUMAN; HUMAN CELL; INSULIN BLOOD LEVEL; MAJOR CLINICAL STUDY; PATIENT COMPLIANCE; POSTMENOPAUSE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN INTAKE; TOMATO; TOMATO JUICE; TUMOR PROMOTION; VITAMIN BLOOD LEVEL; VITAMIN SUPPLEMENTATION;

ADULT; AGED; BREAST NEOPLASMS; CROSS-OVER STUDIES; DIET; FEMALE; HUMANS; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 3; INSULIN-LIKE GROWTH FACTOR BINDING PROTEINS; INSULIN-LIKE GROWTH FACTOR I; INTERVENTION STUDIES; LONGITUDINAL STUDIES; LYCOPERSICON ESCULENTUM; MIDDLE AGED; POSTMENOPAUSE; RISK FACTORS; SOYBEAN PROTEINS;

EID: 79955833956     PISSN: 19406207     EISSN: 19406215     Source Type: Journal    
DOI: 10.1158/1940-6207.CAPR-10-0329     Document Type: Article

References (71)

1. American Cancer Society. Cancer Facts & Figures 2009. Atlanta, GA: American Cancer Society Inc.; 2009.
2. Parkin DM, Bray F, Ferlay J, Pisani P. Estimating the world cancer burden: Globocan 2000. Int J Cancer 2001;94:153-6.
3. Cummings SR, Tice JA, Bauer S, Browner WS, Cuzick J, Ziv E, et al. Prevention of breast cancer in postmenopausal women: approaches to estimating and reducing risk. J Natl Cancer Inst 2009;101:384-98.
4. Waters EA, Cronin KA, Graubard BI, Han PK, Freedman AN. Prevalence of tamoxifen use for breast cancer chemoprevention among U.S. women. Cancer Epidemiol Biomarkers Prev 2010;19;443-6.
5. Doll R, Peto R. The causes of cancer: quantitative estimates of avoidable risks of cancer in the United States today. J Natl Cancer Inst 1981;66:1191-308. (Pubitemid 11063920)
6. World Health Organization. Cancer: Diet and Physical Activity's Impact. Geneva, Switzerland: Noncommunicable Diseases and Mental Health Cluster (NMH), World Health Organization; 2003.
7. Hamajima N, Hirose K, Tajima K, Rohan T, Calle EE, Heath CW Jr., et al. Alcohol, tobacco and breast cancer-collaborative reanalysis of individual data from 53 epidemiological studies, including 58,515 women with breast cancer and 95,067 women without the disease. Br J Cancer 2002;87:1234-45.
8. Key TJ, Verkasalo PK, Banks E. Epidemiology of breast cancer. Lancet Oncol 2001;2:133-40. (Pubitemid 33585924)
9. Key TJ, Allen NE, Spencer EA, Travis RC. Nutrition and breast cancer. Breast 2003;12:412-6. (Pubitemid 38008652)
10. Smith-Warner SA, Spiegelman D, Yaun SS, Adami HO, Beeson WL, Van Den Brandt PA, et al. Intake of fruits and vegetables and risk of breast cancer: a pooled analysis of cohort studies. JAMA 2001;285:769-76. (Pubitemid 32167236)
11. Wu AH, Pike MC, Stram DO. Meta-analysis: dietary fat intake, serum estrogen levels, and the risk of breast cancer. J Natl Cancer Inst 1999;91:529-34. (Pubitemid 29157061)
12. Hankinson SE, Willett WC, Colditz GA, Hunter DJ, Michaud DS, Deroo B, et al. Circulating concentrations of insulin-like growth factor-I and risk of breast cancer. Lancet 1998;351:1393-6. (Pubitemid 28209997)
13. Renehan AG, Zwahlen M, Minder C, O'Dwyer ST, Shalet SM, Egger M. Insulin-like growth factor (IGF)-I, IGF binding protein 3, and cancer risk: systematic review and meta-regression analysis. Lancet 2004;363:1346-53.
14. Toniolo P, Bruning PF, Akhmedkhanov A, Bonfrer JM, Koenig KL, Lukanova A, et al. Serum insulin-like growth factor-I and breast cancer. Int J Cancer 2000;88:828-32.
15. Bohm F, Tinkler JH, Truscott TG. Carotenoids protect against cell membrane damage by the nitrogen dioxide radical. Nat Med 1995;1:98-9.
16. Stahl W, Nicolai S, Briviba K, Hanusch M, Broszeit G, Peters M, et al. Biological activities of natural and synthetic carotenoids: induction of gap junctional communication and singlet oxygen quenching. Carcinogenesis 1997;18:89-92. (Pubitemid 28134620)
17. Zhang LX, Cooney RV, Bertram JS. Carotenoids up-regulate connexin43 gene expression independent of their provitamin A or antioxidant properties. Cancer Res 1992;52:5707-12.
18. Levy J, Bosin E, Feldman B, Giat Y, Miinster A, Danilenko M, et al. Lycopene is a more potent inhibitor of human cancer cell proliferation than either alpha-carotene or beta-carotene. Nutr Cancer 1995;24:257-66.
19. Sharoni Y, Giron E, Rise M, Levy J. Effects of lycopene-enriched tomato oleoresin on 7,12-dimethyl-benz[a]anthracene-induced rat mammary tumors. Cancer Detect Prev 1997;21:118-23. (Pubitemid 27176874)
20. Kucuk O, Sarkar FH, Sakr W, Djuric Z, Pollak MN, Khachik F, et al. Phase II randomized clinical trial of lycopene supplementation before radical prostatectomy. Cancer Epidemiol Biomarkers Prev 2001;10:861-8. (Pubitemid 32738598)
21. Nakachi K, Matusuyama S, Miyake S, Suganuma M, Imai K. Preventive effects of drinking green tea on cancer and cardiovascular disease: epidemiological evidence for multiple targeting prevention. Biofactors 2000;13:49-54. (Pubitemid 32107344)
22. Freudenheim JL, Marshall JR, Vena JE, Laughlin R, Brasure JR, Swanson MK, et al. Premenopausal breast cancer risk and intake of vegetables, fruits, and related nutrients. J Natl Cancer Inst 1996;88:340-8. (Pubitemid 26094240)
23. Potischman N, McCulloch CE, Byers T, Nemoto T, Stubbe N, Milch R, et al. Breast cancer and dietary and plasma concentrations of carotenoids and vitamin A. Am J Clin Nutr 1990;52:909-15.
24. Wane D, Lengacher CA. Integrative review of lycopene and breast cancer. Oncol Nurs Forum 2006;33:127-34.
25. Zhang S, Tang G, Russell RM, Mayzel KA, Stampfer MJ, Willett WC, et al. Measurement of retinoids and carotenoids in breast adipose tissue and a comparison of concentrations in breast cancer cases and control subjects. Am J Clin Nutr 1997;66:626-32. (Pubitemid 27366788)
26. Messina M, McCaskill-Stevens W, Lampe JW. Addressing the soy and breast cancer relationship: review, commentary, and workshop proceedings[review]. J Natl Cancer Inst 2006;98:1275-84. (Pubitemid 44530723)
27. Fournier DB, Erdman JW Jr, Gordon GB. Soy, its components, and cancer prevention: a review of the in vitro, animal, and human data. Cancer Epidemiol Biomarkers Prev 1998;7:1055-65. (Pubitemid 28514109)
28. Chang S, Wu X, Yu H, Spitz MR. Plasma concentrations of insulin-like growth factors among healthy adult men and postmenopausal women: associations with body composition, lifestyle, and reproductive factors. Cancer Epidemiol Biomarkers Prev 2002;11:758-66. (Pubitemid 34851911)
29. Decensi A, Bonanni B, Guerrieri-Gonzaga A, Gandini S, Robertson C, Johansson H, et al. Biologic activity of tamoxifen at low doses in healthy women. J Natl Cancer Inst 1998;90:1461-7. (Pubitemid 28482010)
30. Gann PH, Kazer R, Chatterion R, Gapstur S, Thedford D, Helenowski I, et al. Sequential, randomized trial of a low-fat, high-fiber diet and soy supplementation: Effects on circulating IGF-I and its binding proteins in premenopausal women. Int J Cancer 2005;116:297-303. (Pubitemid 40967269)
31. Horn-Ross PL, John EM, Lee M, Stewart SL, Koo J, Sakoda LC, et al. Phytoestrogen consumption and breast cancer risk in a multiethnic population: the Bay Area Breast Cancer Study. Am J Epidemiol 2001;154:434-41. (Pubitemid 32845481)
32. Shu XO, Zheng Y, Cai H, Gu K, Chen Z, Zheng W, et al. Soy food intake and breast cancer survival. JAMA 2009;302:2437-43.
33. Trock BJ, Hilakivi-Clarke L, Clarke R. Meta-analysis of soy intake and breast cancer risk. J Natl Cancer Inst 2006;98:459-71.
34. Wu AH, Wan P, Hankin J, Tseng C-C, Yu MC, Pike MC. Adolescent and adult soy intake and risk of breast cancer in Asian-Americans. Carcinogenesis 2002;23:1491-6. (Pubitemid 35012429)
35. Yamamoto S, Sobue T, Kobayashi M, Sasaki S, Tsugane S. Soy, isoflavones, and breast cancer risk in Japan. J Natl Cancer Inst 2003;95:906-13. (Pubitemid 36833882)
36. Schairer C, Hill D, Sturgeon SR, Fears T, Pollak M, Mies C, et al. Serum concentrations of IGF-I, IGFBP-3 and C-peptide and risk of hyperplasia and cancer of the breast in postmenopausal women. Int J Cancer 2004;108:773-9. (Pubitemid 38076411)
37. Thompson DJ, Healey CS, Baynes C, Kalmyrzaev B, Ahmed S, Dowsett M, et al. Identification of common variants in the SHBG gene affecting sex hormone-binding globulin levels and breast cancer risk in postmenopausal women. Cancer Epidemiol Biomarkers Prev 2008;17:3490-8.
38. Johnson EJ. The role of carotenoids in human health. Nutr Clin Care 2002;5:56-65.
39. Dai Q, Shu XO, Jin F, Potter JD, Kushi LH, Teas J, et al. Population-based case-control study of soy food intake and breast cancer risk in Shanghai. Br J Cancer 2001;85:372-8. (Pubitemid 32747705)
40. Woodside JV, Campbell MJ, Denholm EE, Newton L, Honour JW, Morton MS, et al. Short-term phytoestrogen supplementation alters insulin-like growth factor profile but not lipid or antioxidant status. J Nutr Biochem 2006;17:211-5. (Pubitemid 43247416)
41. Dewell A, Weidner G, Sumner MD, Barnard RJ, Marlin RO, Daubenmier JJ, et al. Relationship of dietary protein and soy isoflavones to serum IGF-1 and IGF binding proteins in the Prostate Cancer Lifestyle Trial. Nutr Cancer 2007;58:35-42. (Pubitemid 47076160)
42. Khalil DA, Lucas EA, Juma S, Smith BJ, Payton ME, Arjmandi BH. Soy protein supplementation increases serum insulin-like growth factor-I in young and old men but does not affect markers of bone metabolism. J Nutr 2002;132:2605-8. (Pubitemid 35013242)
43. Arjmandi BH, Khalil DA, Smith BJ, Lucas EA, Juma S, Payton ME, et al. Soy protein has a greater effect on bone in postmenopausal women not on hormone replacement therapy, as evidenced by reducing bone resorption and urinary calcium excretion. J Clin Endocrinol Metab 2003;88:1048-54. (Pubitemid 36337755)
44. Maskarinec G, Takata Y, Murphy SP, Franke AA, Kaaks R. Insulin-like growth factor-1 and binding protein-3 in a 2-year soya intervention among premenopausal women. Br J Nutr 2005;94:362-7. (Pubitemid 41404278)
45. Taylor CK, Levy RM, Elliott JC, Burnett BP. The effect of genistein aglycone on cancer and cancer risk: a review of in vitro, preclinical, and clinical studies. Nutr Rev 2009;67:398-415.
46. Velentzis LS, Woodside JV, Cantwell MM, Leathem AJ, Keshtgar MR. Do phytoestrogens reduce the risk of breast cancer and breast cancer recurrence? What clinicians need to know. Eur J Cancer 2008;44:1799-806.
47. Adlercreutz H, Mazur W. Phyto-oestrogens and Western diseases. Ann Med 1997;29:95-120. (Pubitemid 27226319)
48. Li Z, Wang Y, Mo B. [The effects of carotenoids on the proliferation of human breast cancer cell and gene expression of bcl-2]. Zhonghua yu fang yi xue za zhi[Chinese J Prev Med] 2002;36:254-7 [abstract].
49. Prakash P, Russell RM, Krinsky NI. In vitro inhibition of proliferation of estrogen-dependent and estrogen-independent human breast cancer cells treated with carotenoids or retinoids. J Nutr 2001;131:1574-80.
50. Amir H, Karas M, Giat J, Danilenko M, Levy R, Yermiahu T, et al. Lycopene and 1,25-dihydroxyvitamin D3 cooperate in the inhibition of cell cycle progression and induction of differentiation in HL-60 leukemic cells. Nutr Cancer 1999;33:105-12. (Pubitemid 29196131)
51. Nahum A, Hirsch K, Danilenko M, Watts CK, Prall OW, Levy J, et al. Lycopene inhibition of cell cycle progression in breast and endometrial cancer cells is associated with reduction in cyclin D levels and retention of p27(Kip1) in the cyclin E-cdk2 complexes. Oncogene 2001;20:3428-36. (Pubitemid 32588991)
52. Zhang LX, Cooney RV, Bertram JS. Carotenoids enhance gap junctional communication and inhibit lipid peroxidation in C3H/10T1/2 cells: relationship to their cancer chemopreventive action. Carcinogenesis 1991;12:2109-14.
53. Nagasawa H, Mitamura T, Sakamoto S, Yamamoto K. Effects of lycopene on spontaneous mammary tumour development in SHN virgin mice. Anticancer Res 1995;15:1173-8.
54. Gandini S, Merzenich H, Robertson C, Boyle P. Meta-analysis of studies on breast cancer risk and diet: the role of fruit and vegetable consumption and the intake of associated micronutrients. Eur J Cancer 2000;36:636-46. (Pubitemid 30156850)
55. McEligot AJ, Rock CL, Flatt SW, Newman V, Faerber S, Pierce JP. Plasma carotenoids are biomarkers of long-term high vegetable intake in women with breast cancer. J Nutr 1999;129:2258-63.
56. Pool-Zobel BL, Bub A, Muller H, Wollowski I, Rechkemmer G. Consumption of vegetables reduces genetic damage in humans: first results of a human intervention trial with carotenoid-rich foods. Carcinogenesis 1997;18:1847-50. (Pubitemid 28134695)
57. Nagata C, Shimizu H, Takami R, Hayashi M, Takeda N, Yasuda K. Dietary soy and fats in relation to serum insulin-like growth factor-1 and insulin-like growth factor-binding protein-3 levels in premenopausal Japanese women. Nutr Cancer 2003;45:185-9. (Pubitemid 37022791)
58. Vrieling A, Voskuil DW, Bueno de Mesquita HB, Kaaks R, van Noord PA, Keinan-Boker L, et al. Dietary determinants of circulating insulin-like growth factor (IGF)-I and IGF binding proteins 1, -2 and -3 in women in the Netherlands. Cancer Causes Control 2004;15:787-96. (Pubitemid 39335575)
59. Duffy C, Cyr M. Phytoestrogens: potential benefits and implications for breast cancer survivors. J Womens Health (Larchmt) 2003;12:617-31. (Pubitemid 37266005)
60. Guha N, Kwan ML, Quesenberry CP Jr, Weltzien EK, Castillo AL, Caan BJ. Soy isoflavones and risk of cancer recurrence in a cohort of breast cancer survivors: the Life After Cancer Epidemiology study. Breast Cancer Res Treat 2009;118:395-405.
61. Lu LJ, Anderson KE, Grady JJ, Kohen F, Nagamani M. Decreased ovarian hormones during a soya diet: implications for breast cancer prevention. Cancer Res 2000;60:4112-21. (Pubitemid 30636593)
62. Lu LJ, Cree M, Josyula S, Nagamani M, Grady JJ, Anderson KE. Increased urinary excretion of 2-hydroxyestrone but not 16alphahydroxyestrone in premenopausal women during a soya diet containing isoflavones. Cancer Res 2000;60:1299-305. (Pubitemid 30151998)
63. McMichael-Phillips DF, Harding C, Morton M, Roberts SA, Howell A, Potten CS, et al. Effects of soy-protein supplementation on epithelial proliferation in the histologically normal human breast. Am J Clin Nutr 1998;68:1431S-5S.
64. Nagata C, Takatsuka N, Inaba S, Kawakami N, Shimizu H. Effect of soymilk consumption on serum estrogen concentrations in premenopausal Japanese women. J Natl Cancer Inst 1998;90:1830-5. (Pubitemid 28559896)
65. Wu AH, Stanczyk FZ, Hendrich S, Murphy PA, Zhang C, Wan P, et al. Effects of soy foods on ovarian function in premenopausal women. Br J Cancer 2000;82:1879-86. (Pubitemid 30307405)
66. Baglietto L, English DR, Hopper JL, Morris HA, Tilley WD, Giles GG. Circulating insulin-like growth factor-I and binding protein-3 and the risk of breast cancer. Cancer Epidemiol Biomarkers Prev 2007;16:763-8. (Pubitemid 46650579)
67. Rinaldi S, Peeters PH, Berrino F, Dossus L, Biessy C, Olsen A, et al. IGF-I, IGFBP-3 and breast cancer risk in women: The European Prospective Investigation into Cancer and Nutrition (EPIC). Endocr Relat Cancer 2006;13:593-605.
68. Schernhammer ES, Holly JM, Hunter DJ, Pollak MN, Hankinson SE. Insulin-like growth factor-I, its binding proteins (IGFBP-1 and IGFBP-3), and growth hormone and breast cancer risk in The Nurses Health Study II. Endocr Relat Cancer 2006;13:583-92. (Pubitemid 43886678)
69. Jakes RW, Duffy SW, Ng F-C, Gao F, Ng E-H, Seow A, et al. Mammographic parenchymal patterns and self-reported soy intake in Singapore Chinese women. Cancer Epidemiol Biomarkers Prev 2002;11:608-13. (Pubitemid 34760818)
70. Adami HO, Signorello LB, Trichopoulos D. Towards an understanding of breast cancer etiology. Semin Cancer Biol 1998;8:255-62. (Pubitemid 28550383)
71. Hilakivi-Clarke L, Cabanes A, Olivo S, Kerr L, Bouker KB, Clarke R. Do estrogens always increase breast cancer risk? J Steroid Biochem Mol Biol 2002;80:163-74.