Dietary compared with blood concentrations of carotenoids and breast cancer risk: A systematic review and meta-analysis of prospective studies

American Journal of Clinical Nutrition

Volumn 96, Issue 2, 2012, Pages 356-373

  Aune, Dagfinn ^a   Chan, Doris S M ^a   Vieira, Ana Rita ^a   Navarro Rosenblatt, Deborah A ^a   Vieira, Rui ^a   Greenwood, Darren C ^b   Norat, Teresa ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA CAROTENE; BETA CAROTENE; BETA CRYPTOXANTHIN; BIOLOGICAL MARKER; CAROTENOID; XANTHOPHYLL; ZEAXANTHIN;

ARTICLE; BLOOD LEVEL; BREAST CANCER; CANCER RISK; DIET SUPPLEMENTATION; DIETARY INTAKE; FOOD FREQUENCY QUESTIONNAIRE; FRUIT; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; RISK REDUCTION; SYSTEMATIC REVIEW; VEGETABLE;

BETA CAROTENE; BIOLOGICAL MARKERS; BREAST NEOPLASMS; CAROTENOIDS; DIET; DIETARY SUPPLEMENTS; FEMALE; FRUIT; HUMANS; LUTEIN; RISK FACTORS; VEGETABLES; XANTHOPHYLLS;

EID: 84864336704     PISSN: 00029165     EISSN: 19383207     Source Type: Journal    
DOI: 10.3945/ajcn.112.034165     Document Type: Article

References (81)

1. Steinmetz KA, Potter JD. Vegetables, fruit, and cancer. I. Epidemiology. Cancer Causes Control 1991;2:325-57.
2. Steinmetz KA, Potter JD. Vegetables, fruit, and cancer. II. Mechanisms. Cancer Causes Control 1991;2:427-42.
3. Smith-Warner SA, Spiegelman D, Yaun SS, Adami HO, Beeson WL, van den Brandt PA, Folsom AR, Fraser GE, Freudenheim JL, Goldbohm RA, 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)
4. van Gils CH, Peeters PH, Bueno-de-Mesquita HB, Boshuizen HC, Lahmann PH, Clavel-Chapelon F, Thiebaut A, Kesse E, Sieri S, Palli D, et al. Consumption of vegetables and fruits and risk of breast cancer. JAMA 2005;293:183-93. (Pubitemid 40095869)
5. George SM, Park Y, Leitzmann MF, Freedman ND, Dowling EC, Reedy J, Schatzkin A, Hollenbeck A, Subar AF. Fruit and vegetable intake and risk of cancer: a prospective cohort study. Am J Clin Nutr 2009;89:347-53.
6. Brasky TM, Lampe JW, Potter JD, Patterson RE, White E. Specialty supplements and breast cancer risk in the VITamins And Lifestyle (VITAL) Cohort. Cancer Epidemiol Biomarkers Prev 2010;19:1696-708.
7. Boggs DA, Palmer JR, Wise LA, Spiegelman D, Stampfer MJ, Adams- Campbell LL, Rosenberg L. Fruit and vegetable intake in relation to risk of breast cancer in the Black Women's Health Study. Am J Epidemiol 2010;172:1268-79.
8. World Cancer Research Fund/American Insitute for Cancer Research. Food, nutrition, physical activity and the prevention of cancer: a global perspective. Washington, DC: AICR, 2007.
9. Kristal AR, Peters U, Potter JD. Is it time to abandon the food frequency questionnaire? Cancer Epidemiol Biomarkers Prev 2005;14: 2826-8. (Pubitemid 43068811)
10. Kristal AR, Potter JD. Not the time to abandon the food frequency questionnaire: counterpoint. Cancer Epidemiol Biomarkers Prev 2006; 15:1759-60. (Pubitemid 44664245)
11. Kipnis V, Subar AF, Midthune D, Freedman LS, Ballard-Barbash R, Troiano RP, Bingham S, Schoeller DA, Schatzkin A, Carroll RJ. Structure of dietary measurement error: results of the OPEN biomarker study. Am J Epidemiol 2003;158:14-21. (Pubitemid 36745326)
12. Bingham SA, Day NE, Luben R, Ferrari P, Slimani N, Norat T, Clavel-Chapelon F, Kesse E, Nieters A, Boeing H, et al. Dietary fibre in food and protection against colorectal cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC): an observational study. Lancet 2003;361:1496-501. (Pubitemid 36566339)
13. Park Y, Hunter DJ, Spiegelman D, Bergkvist L, Berrino F, van den Brandt PA, Buring JE, Colditz GA, Freudenheim JL, Fuchs CS, et al. Dietary fiber intake and risk of colorectal cancer: a pooled analysis of prospective cohort studies. JAMA 2005;294:2849-57. (Pubitemid 41785865)
14. Park Y, Brinton LA, Subar AF, Hollenbeck A, Schatzkin A. Dietary fiber intake and risk of breast cancer in postmenopausal women: the National Institutes of Health-AARP Diet and Health Study. Am J Clin Nutr 2009;90:664-71.
15. Norat T, Bingham S, Ferrari P, Slimani N, Jenab M, Mazuir M, Overvad K, Olsen A, Tjonneland A, Clavel F, et al. Meat, fish, and colorectal cancer risk: the European Prospective Investigation Into Cancer and Nutrition. J Natl Cancer Inst 2005;97:906-16. (Pubitemid 41417942)
16. Dahm CC, Keogh RH, Spencer EA, Greenwood DC, Key TJ, Fentiman IS, Shipley MJ, Brunner EJ, Cade JE, Burley VJ, et al. Dietary fiber and colorectal cancer risk: a nested case-control study using food diaries. J Natl Cancer Inst 2010;102:614-26.
17. Prentice RL, Shaw PA, Bingham SA, Beresford SA, Caan B, Neuhouser ML, Patterson RE, Stefanick ML, Satterfield S, Thomson CA, et al. Biomarker-calibrated energy and protein consumption and increased cancer risk among postmenopausal women. Am J Epidemiol 2009;169:977-89.
18. Bingham SA, Luben R, Welch A, Wareham N, Khaw KT, Day N. Are imprecise methods obscuring a relation between fat and breast cancer? Lancet 2003;362:212-4. (Pubitemid 36859940)
19. Freedman LS, Potischman N, Kipnis V, Midthune D, Schatzkin A, Thompson FE, Troiano RP, Prentice R, Patterson R, Carroll R, et al. A comparison of two dietary instruments for evaluating the fat-breast cancer relationship. Int J Epidemiol 2006;35:1011-21. (Pubitemid 44540756)
20. Jenab M, Riboli E, Ferrari P, Sabate J, Slimani N, Norat T, Friesen M, Tjonneland A, Olsen A, Overvad K, et al. Plasma and dietary vitamin C levels and risk of gastric cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC-EURGAST). Carcinogenesis 2006;27:2250-7. (Pubitemid 44644814)
21. Jenab M, Riboli E, Ferrari P, Friesen M, Sabate J, Norat T, Slimani N, Tjonneland A, Olsen A, Overvad K, et al. Plasma and dietary carotenoid, retinol and tocopherol levels and the risk of gastric adenocarcinomas in the European prospective investigation into cancer and nutrition. Br J Cancer 2006;95:406-15. (Pubitemid 44187608)
22. Harding AH, Wareham NJ, Bingham SA, Khaw K, Luben R, Welch A, Forouhi NG. Plasma vitamin C level, fruit and vegetable consumption, and the risk of new-onset type 2 diabetes mellitus: the European prospective investigation of cancer-Norfolk prospective study. Arch Intern Med 2008;168:1493-9.
23. Bingham S, Luben R, Welch A, Low YL, Khaw KT, Wareham N, Day N. Associations between dietary methods and biomarkers, and between fruits and vegetables and risk of ischaemic heart disease, in the EPIC Norfolk Cohort Study. Int J Epidemiol 2008;37:978-87.
24. Freedman LS, Schatzkin A, Midthune D, Kipnis V. Dealing with dietary measurement error in nutritional cohort studies. J Natl Cancer Inst 2011;103:1086-92.
25. Al-Delaimy WK, Ferrari P, Slimani N, Pala V, Johansson I, Nilsson S, Mattisson I, Wirfalt E, Galasso R, Palli D, et al. Plasma carotenoids as biomarkers of intake of fruits and vegetables: individual-level correlations in the European Prospective Investigation into Cancer and Nutrition (EPIC). Eur J Clin Nutr 2005;59:1387-96. (Pubitemid 43135154)
26. Hodge AM, Simpson JA, Fridman M, Rowley K, English DR, Giles GG, Su Q, O'Dea K. Evaluation of an FFQ for assessment of antioxidant intake using plasma biomarkers in an ethnically diverse population. Public Health Nutr 2009;12:2438-47.
27. Polsinelli ML, Rock CL, Henderson SA, Drewnowski A. Plasma carotenoids as biomarkers of fruit and vegetable servings in women. JAm Diet Assoc 1998;98:194-6. (Pubitemid 28078257)
28. Smith-Warner SA, Elmer PJ, Tharp TM, Fosdick L, Randall B, Gross M, Wood J, Potter JD. Increasing vegetable and fruit intake: randomized intervention and monitoring in an at-risk population. Cancer Epidemiol Biomarkers Prev 2000;9:307-17. (Pubitemid 30165444)
29. Macdonald HM, Hardcastle AC, Duthie GG, Duthie SJ, Aucott L, Sandison R, Shearer MJ, Reid DM. Changes in vitamin biomarkers during a 2-year intervention trial involving increased fruit and vegetable consumption by free-living volunteers. Br J Nutr 2009;102:1477-86.
30. Carlsen MH, Karlsen A, Lillegaard IT, Gran JM, Drevon CA, Blomhoff R, Andersen LF. Relative validity of fruit and vegetable intake estimated from an FFQ, using carotenoid and flavonoid biomarkers and the method of triads. Br J Nutr 2011;105:1530-8.
31. Cui Y, Shikany JM, Liu S, Shagufta Y, Rohan TE. Selected antioxidants and risk of hormone receptor-defined invasive breast cancers among postmenopausal women in the Women's Health Initiative Observational Study. Am J Clin Nutr 2008;87:1009-18. (Pubitemid 351549247)
32. Shibata A, Paganini-Hill A, Ross RK, Henderson BE. Intake of vegetables, fruits, beta-carotene, vitamin C and vitamin supplements and cancer incidence among the elderly: a prospective study. Br J Cancer 1992;66:673-9.
33. Graham S, Zielezny M, Marshall J, Priore R, Freudenheim J, Brasure J, Haughey B, Nasca P, Zdeb M. Diet in the epidemiology of postmenopausal breast cancer in the New York State Cohort. Am J Epidemiol 1992;136:1327-37. (Pubitemid 23046417)
34. Kushi LH, Fee RM, Sellers TA, Zheng W, Folsom AR. Intake of vitamins A, C, and E and postmenopausal breast cancer. The Iowa Women's Health Study. Am J Epidemiol 1996;144:165-74. (Pubitemid 26234995)
35. Verhoeven DT, Assen N, Goldbohm RA, Dorant E, van't Veer P, Sturmans F, Hermus RJ, van den Brandt PA. Vitamins C and E, retinol, beta-carotene and dietary fibre in relation to breast cancer risk: a prospective cohort study. Br J Cancer 1997;75:149-55. (Pubitemid 27007289)
36. Zhang S, Hunter DJ, Forman MR, Rosner BA, Speizer FE, Colditz GA, Manson JE, Hankinson SE, Willett WC. Dietary carotenoids and vitamins A, C, and E and risk of breast cancer. J Natl Cancer Inst 1999; 91:547-56. (Pubitemid 29157064)
37. Terry P, Jain M, Miller AB, Howe GR, Rohan TE. Dietary carotenoids and risk of breast cancer. Am J Clin Nutr 2002;76:883-8.
38. Horn-Ross PL, Hoggatt KJ, West DW, Krone MR, Stewart SL, Anton H, Bernstei CL, Deapen D, Peel D, Pinder R, et al. Recent diet and breast cancer risk: the California Teachers Study (USA). Cancer Causes Control 2002;13:407-15. (Pubitemid 34666596)
39. Cho E, Spiegelman D, Hunter DJ, Chen WY, Zhang SM, Colditz GA, Willett WC. Premenopausal intakes of vitamins A, C, and E, folate, and carotenoids, and risk of breast cancer. Cancer Epidemiol Biomarkers Prev 2003;12:713-20. (Pubitemid 36993160)
40. Nagel G, Linseisen J, van Gils CH, Peeters PH, Boutron-Ruault MC, Clavel-Chapelon F, Romieu I, Tjonneland A, Olsen A, Roswall N, et al. Dietary beta-carotene, vitamin C and E intake and breast cancer risk in the European Prospective Investigation into Cancer and Nutrition (EPIC). Breast Cancer Res Treat 2010;119:753-65.
41. Larsson SC, Bergkvist L, Wolk A. Dietary carotenoids and risk of hormone receptor-defined breast cancer in a prospective cohort of Swedish women. Eur J Cancer 2010;46:1079-85.
42. Wald NJ, Boreham J, Hayward JL, Bulbrook RD. Plasma retinol, betacarotene and vitamin E levels in relation to the future risk of breast cancer. Br J Cancer 1984;49:321-4. (Pubitemid 14165329)
43. Toniolo P, Van Kappel AL, Akhmedkhanov A, Ferrari P, Kato I, Shore RE, Riboli E. Serum carotenoids and breast cancer. Am J Epidemiol 2001;153:1142-7. (Pubitemid 32552269)
44. Hultén K, Van Kappel AL, Winkvist A, Kaaks R, Hallmans G, Lenner P, Riboli E. Carotenoids, alpha-tocopherols, and retinol in plasma and breast cancer risk in northern Sweden. Cancer Causes Control 2001;12:529-37. (Pubitemid 32735125)
45. Sato R, Helzlsouer KJ, Alberg AJ, Hoffman SC, Norkus EP, Comstock GW. Prospective study of carotenoids, tocopherols, and retinoid concentrations and the risk of breast cancer. Cancer Epidemiol Biomarkers Prev 2002;11:451-7. (Pubitemid 34517940)
46. Tamimi RM, Hankinson SE, Campos H, Spiegelman D, Zhang S, Colditz GA, Willett WC, Hunter DJ. Plasma carotenoids, retinol, and tocopherols and risk of breast cancer. Am J Epidemiol 2005;161:153-60. (Pubitemid 40096790)
47. Kabat GC, Kim M, Adams-Campbell LL, Caan BJ, Chlebowski RT, Neuhouser ML, Shikany JM, Rohan TE. Longitudinal study of serum carotenoid, retinol, and tocopherol concentrations in relation to breast cancer risk among postmenopausal women. Am J Clin Nutr 2009;90:162-9.
48. Epplein M, Shvetsov YB, Wilkens LR, Franke AA, Cooney RV, Le Marchand L, Henderson BE, Kolonel LN, Goodman MT. Plasma carotenoids, retinol, and tocopherols and postmenopausal breast cancer risk in the Multiethnic Cohort Study: a nested case-control study. Breast Cancer Res 2009;11:R49.
49. Maillard V, Kuriki K, Lefebvre B, Boutron-Ruault MC, Lenoir GM, Joulin V, Clavel-Chapelon F, Chajes V. Serum carotenoid, tocopherol and retinol concentrations and breast cancer risk in the E3N-EPIC study. Int J Cancer 2010;127:1188-96.
50. Knekt P, Aromaa A, Maatela J, Aaran RK, Nikkari T, Hakama M, Hakulinen T, Peto R, Teppo L. Serum vitamin A and subsequent risk of cancer: cancer incidence follow-up of the Finnish Mobile Clinic Health Examination Survey. Am J Epidemiol 1990;132:857-70. (Pubitemid 20363664)
51. Comstock GW, Helzlsouer KJ, Bush TL. Prediagnostic serum levels of carotenoids and vitamin E as related to subsequent cancer in Washington County, Maryland. Am J Clin Nutr 1991;53:260S-4S.
52. Dorgan JF, Sowell A, Swanson CA, Potischman N, Miller R, Schussler N, Stephenson HE Jr. Relationships of serum carotenoids, retinol, alpha-tocopherol, and selenium with breast cancer risk: results from a prospective study in Columbia, Missouri (United States). Cancer Causes Control 1998;9:89-97. (Pubitemid 28048664)
53. Sesso HD, Buring JE, Zhang SM, Norkus EP, Gaziano JM. Dietary and plasma lycopene and the risk of breast cancer. Cancer Epidemiol Biomarkers Prev 2005;14:1074-81. (Pubitemid 40656450)
54. Dorjgochoo T, Gao YT, Chow WH, Shu XO, Li H, Yang G, Cai Q, Rothman N, Cai H, Franke AA, et al. Plasma carotenoids, tocopherols, retinol and breast cancer risk: results from the Shanghai Women Health Study (SWHS). Breast Cancer Res Treat 2009;117:381-9.
55. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, Moher D, Becker BJ, Sipe TA, Thacker SB. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Metaanalysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA 2000;283:2008-12. (Pubitemid 30214957)
56. Rohan TE, Howe GR, Friedenreich CM, Jain M, Miller AB. Dietary fiber, vitamins A, C, and E, and risk of breast cancer: a cohort study. Cancer Causes Control 1993;4:29-37. (Pubitemid 23051895)
57. Giovannucci E, Stampfer MJ, Colditz GA, Manson JE, Rosner BA, Longnecker M, Speizer FE, Willett WC. A comparison of prospective and retrospective assessments of diet in the study of breast cancer. Am J Epidemiol 1993;137:502-11. (Pubitemid 23109751)
58. Hunter DJ, Manson JE, Colditz GA, Stampfer MJ, Rosner B, Hennekens CH, Speizer FE, Willett WC. A prospective study of the intake of vitamins C, E, and A and the risk of breast cancer. N Engl J Med 1993;329:234-40. (Pubitemid 23203814)
59. Jumaan AO, Holmberg L, Zack M, Mokdad AH, Ohlander EM, Wolk A, Byers T. Beta-carotene intake and risk of postmenopausal breast cancer. Epidemiology 1999;10:49-53. (Pubitemid 29014428)
60. Michels KB, Holmberg L, Bergkvist L, Ljung H, Bruce A, Wolk A. Dietary antioxidant vitamins, retinol, and breast cancer incidence in a cohort of Swedish women. Int J Cancer 2001;91:563-7. (Pubitemid 32115114)
61. Frazier AL, Ryan CT, Rockett H, Willett WC, Colditz GA. Adolescent diet and risk of breast cancer. Breast Cancer Res 2003;5:R59-64.
62. Roswall N, Olsen A, Christensen J, Dragsted LO, Overvad K, Tjonneland A. Micronutrient intake and breast cancer characteristics among postmenopausal women. Eur J Cancer Prev 2010;19:360-5.
63. Han J, Hankinson SE, De Vivo I, Spiegelman D, Tamimi RM, Mohrenweiser HW, Colditz GA, Hunter DJ. A prospective study of XRCC1 haplotypes and their interaction with plasma carotenoids on breast cancer risk. Cancer Res 2003;63:8536-41. (Pubitemid 37549513)
64. Tamimi RM, Hankinson SE, Spiegelman D, Colditz GA, Hunter DJ. Manganese superoxide dismutase polymorphism, plasma antioxidants, cigarette smoking, and risk of breast cancer. Cancer Epidemiol Biomarkers Prev 2004;13:989-96. (Pubitemid 38756709)
65. Tamimi RM, Colditz GA, Hankinson SE. Circulating carotenoids, mammographic density, and subsequent risk of breast cancer. Cancer Res 2009;69:9323-9.
66. He C, Tamimi RM, Hankinson SE, Hunter DJ, Han J. A prospective study of genetic polymorphism in MPO, antioxidant status, and breast cancer risk. Breast Cancer Res Treat 2009;113:585-94.
67. DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials 1986;7:177-88. (Pubitemid 17189972)
68. Aune D, Lau R, Chan DS, Vieira R, Greenwood DC, Kampman E, Norat T. Nonlinear reduction in risk for colorectal cancer by fruit and vegetable intake based on meta-analysis of prospective studies. Gastroenterology 2011;141:106-18.
69. Greenland S, Longnecker MP. Methods for trend estimation from summarized dose-response data, with applications to meta-analysis. Am J Epidemiol 1992;135:1301-9.
70. Switzer BR, Atwood JR, Stark AH, Hatch JW, Travis R, Ullrich F, Lyden ER, Wu X, Chiu Y, Smith JL. Plasma carotenoid and vitamins A and E concentrations in older African American women after wheat bran supplementation: effects of age, body mass and smoking history. J Am Coll Nutr 2005;24:217-26. (Pubitemid 41201965)
71. Royston P. A strategy for modelling the effect of a continuous covariate in medicine and epidemiology. Stat Med 2000;19:1831-47. (Pubitemid 30448192)
72. Bagnardi V, Zambon A, Quatto P, Corrao G. Flexible meta-regression functions for modeling aggregate dose-response data, with an application to alcohol and mortality. Am J Epidemiol 2004;159:1077-86.
73. Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med 2002;21:1539-58. (Pubitemid 34746062)
74. Egger M, Davey SG, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997;315:629-34. (Pubitemid 27387172)
75. Zhang X, Spiegelman D, Baglietto L, Bernstein L, Boggs DA, van den Brandt PA, Buring JE, Gapstur SM, Giles GG, Giovannucci E, et al. Carotenoid intakes and risk of breast cancer defined by estrogen receptor and progesterone receptor status: a pooled analysis of 18 prospective cohort studies. Am J Clin Nutr 2012;95:713-25.
76. Jenab M, Slimani N, Bictash M, Ferrari P, Bingham SA. Biomarkers in nutritional epidemiology: applications, needs and new horizons. Hum Genet 2009;125:507-25.
77. Hua S, Kittler R, White KP. Genomic antagonism between retinoic acid and estrogen signaling in breast cancer. Cell 2009;137:1259-71.
78. Cui Y, Lu Z, Bai L, Shi Z, Zhao WE, Zhao B. beta-Carotene induces apoptosis and up-regulates peroxisome proliferator-activated receptor gamma expression and reactive oxygen species production in MCF-7 cancer cells. Eur J Cancer 2007;43:2590-601. (Pubitemid 350086930)
79. Tang XH, Gudas LJ. Retinoids, retinoic acid receptors, and cancer. Annu Rev Pathol 2011;6:345-64.
80. Aune D, Chan DS, Greenwood DC, Vieira AR, Rosenblatt DA, Vieira R, Norat T. Dietary fiber and breast cancer risk: a systematic review and meta-analysis of prospective studies. Ann Oncol 2012;23:1394-402.
81. Liu RH. Potential synergy of phytochemicals in cancer prevention: mechanism of action. J Nutr 2004;134(12 suppl):3479S-85S. (Pubitemid 39587593)