Dairy products, calcium, and prostate cancer risk: A systematic review and meta-analysis of cohort studies

American Journal of Clinical Nutrition

Volumn 101, Issue 1, 2015, Pages 87-117

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

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

Calcium; Dairy products; Milk; Prostate cancer; WCRF AICR continuous update project

Indexed keywords

ALPHA TOCOPHEROL; BETA CAROTENE; CALCIUM; FAT; MILK FAT; YOGHURT; CALCIUM INTAKE;

ARTICLE; BUTTER; CALCIUM INTAKE; CANCER RISK; DAIRY PRODUCT; HUMAN; ICE CREAM; MALE; MILK; PROSTATE CANCER; SYSTEMATIC REVIEW; COHORT ANALYSIS; COMPARATIVE STUDY; DIET SUPPLEMENTATION; INCIDENCE; META ANALYSIS; MORTALITY; PROSPECTIVE STUDY; PROSTATIC NEOPLASMS; RISK FACTOR;

CALCIUM, DIETARY; COHORT STUDIES; DAIRY PRODUCTS; DIETARY SUPPLEMENTS; HUMANS; INCIDENCE; MALE; PROSPECTIVE STUDIES; PROSTATIC NEOPLASMS; RISK FACTORS;

EID: 84919665425     PISSN: 00029165     EISSN: 19383207     Source Type: Journal    
DOI: 10.3945/ajcn.113.067157     Document Type: Article

References (86)

1. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 2010;127:2893-917.
2. Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin 2005;55:74-108.
3. Lee J, Demissie K, Lu SE, Rhoads GG. Cancer incidence among Korean-American immigrants in the United States and native Koreans in South Korea. Cancer Control 2007;14:78-85.
4. Maskarinec G, Noh JJ. The effect of migration on cancer incidence among Japanese in Hawaii. Ethn Dis 2004;14:431-9.
5. Shimizu H, Ross RK, Bernstein L, Yatani R, Henderson BE, Mack TM. Cancers of the prostate and breast among Japanese and white immigrants in Los Angeles County. Br J Cancer 1991;63:963-6.
6. Hsing AW, Devesa SS, Jin F, Gao YT. Rising incidence of prostate cancer in Shanghai, China. Cancer Epidemiol Biomarkers Prev 1998;7: 83-4.
7. Hsing AW, Tsao L, Devesa SS. International trends and patterns of prostate cancer incidence and mortality. Int J Cancer 2000;85:60-7.
8. Ganmaa D, Li XM, Qin LQ, Wang PY, Takeda M, Sato A. The experience of Japan as a clue to the etiology of testicular and prostatic cancers. Med Hypotheses 2003;60:724-30.
9. 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.
10. Ganmaa D, Li XM, Wang J, Qin LQ, Wang PY, Sato A. Incidence and mortality of testicular and prostatic cancers in relation to world dietary practices. Int J Cancer 2002;98:262-7.
11. Zhang J, Kesteloot H. Milk consumption in relation to incidence of prostate, breast, colon, and rectal cancers: is there an independent effect? Nutr Cancer 2005;53:65-72.
12. Grant WB. An ecologic study of dietary links to prostate cancer. Altern Med Rev 1999;4:162-9.
13. Aune D, Lau R, Chan DS, Vieira R, Greenwood DC, Kampman E, Norat T. Dairy products and colorectal cancer risk: a systematic review and meta-analysis of cohort studies. Ann Oncol 2012;23:37-45.
14. Severi G, English DR, Hopper JL, Giles GG. Re: Prospective studies of dairy product and calcium intakes and prostate cancer risk: a metaanalysis. J Natl Cancer Inst 2006;98:794-5.
15. Koh KA, Sesso HD, Paffenbarger RS Jr, Lee IM. Dairy products, calcium and prostate cancer risk. Br J Cancer 2006;95:1582-5.
16. Kesse E, Bertrais S, Astorg P, Jaouen A, Arnault N, Galan P, Hercberg S. Dairy products, calcium and phosphorus intake, and the risk of prostate cancer: results of the French prospective SU.VI.MAX (Supplementation en Vitamines et Mineraux Antioxydants) study. Br J Nutr 2006;95:539-45.
17. Giovannucci E, Liu Y, Stampfer MJ, Willett WC. A prospective study of calcium intake and incident and fatal prostate cancer. Cancer Epidemiol Biomarkers Prev 2006;15:203-10.
18. Tande AJ, Platz EA, Folsom AR. The metabolic syndrome is associated with reduced risk of prostate cancer. Am J Epidemiol 2006;164:1094-102.
19. Rohrmann S, Platz EA, Kavanaugh CJ, Thuita L, Hoffman SC, Helzlsouer KJ. Meat and dairy consumption and subsequent risk of prostate cancer in a US cohort study. Cancer Causes Control 2007;18: 41-50.
20. Neuhouser ML, Barnett MJ, Kristal AR, Ambrosone CB, King I, Thornquist M, Goodman G. (n-6) PUFA increase and dairy foods decrease prostate cancer risk in heavy smokers. J Nutr 2007;137:1821-7.
21. Park SY, Murphy SP, Wilkens LR, Stram DO, Henderson BE, Kolonel LN. Calcium, vitamin D, and dairy product intake and prostate cancer risk: the Multiethnic Cohort Study. Am J Epidemiol 2007;166:1259-69.
22. Park Y, Mitrou PN, Kipnis V, Hollenbeck A, Schatzkin A, Leitzmann MF. Calcium, dairy foods, and risk of incident and fatal prostate cancer: the NIH-AARP Diet and Health Study. Am J Epidemiol 2007; 166:1270-9.
23. Mitrou PN, Albanes D, Weinstein SJ, Pietinen P, Taylor PR, Virtamo J, Leitzmann MF. A prospective study of dietary calcium, dairy products and prostate cancer risk (Finland). Int J Cancer 2007;120:2466-73.
24. Ahn J, Albanes D, Peters U, Schatzkin A, Lim U, Freedman M, Chatterjee N, Andriole GL, Leitzmann MF, Hayes RB. Dairy products, calcium intake, and risk of prostate cancer in the prostate, lung, colorectal, and ovarian cancer screening trial. Cancer Epidemiol Biomarkers Prev 2007;16:2623-30.
25. Iso H, Kubota Y. Nutrition and disease in the Japan Collaborative Cohort Study for Evaluation of Cancer (JACC). Asian Pac J Cancer Prev 2007;8(Suppl):35-80.
26. Kurahashi N, Inoue M, Iwasaki M, Sasazuki S, Tsugane AS. Dairy product, saturated fatty acid, and calcium intake and prostate cancer in a prospective cohort of Japanese men. Cancer Epidemiol Biomarkers Prev 2008;17:930-7.
27. Allen NE, Key TJ, Appleby PN, Travis RC, Roddam AW, Tjonneland A, Johnsen NF, Overvad K, Linseisen J, Rohrmann S, et al. Animal foods, protein, calcium and prostate cancer risk: the European Prospective Investigation into Cancer and Nutrition. Br J Cancer 2008;98:1574-81.
28. Park Y, Leitzmann MF, Subar AF, Hollenbeck A, Schatzkin A. Dairy food, calcium, and risk of cancer in the NIH-AARP Diet and Health Study. Arch Intern Med 2009;169:391-401.
29. Chae YK, Huang HY, Strickland P, Hoffman SC, Helzlsouer K. Genetic polymorphisms of estrogen receptors alpha and beta and the risk of developing prostate cancer. PLoS ONE 2009;4:e6523.
30. Butler LM, Wong AS, Koh WP, Wang R, Yuan JM, Yu MC. Calcium intake increases risk of prostate cancer among Singapore Chinese. Cancer Res 2010;70:4941-8.
31. Kristal AR, Arnold KB, NeuhouserML, Goodman P, Platz EA, Albanes D, Thompson IM. Diet, supplement use, and prostate cancer risk: results from the prostate cancer prevention trial. Am J Epidemiol 2010;172:566-77.
32. Song Y, Chavarro JE, Cao Y, QiuW, Mucci L, Sesso HD, Stampfer MJ, Giovannucci E, Pollak M, Liu S, et al. Whole milk intake is associated with prostate cancer-specific mortality among US male physicians. J Nutr 2013;143:189-96.
33. Torfadottir JE, Steingrimsdottir L, Mucci L, Aspelund T, Kasperzyk JL, Olafsson O, Fall K, Tryggvadottir L, Harris TB, Launer L, et al. Milk intake in early life and risk of advanced prostate cancer. Am J Epidemiol 2012;175:144-53.
34. Giovannucci E, Liu Y, Platz EA, Stampfer MJ, Willett WC. Risk factors for prostate cancer incidence and progression in the health professionals follow-up study. Int J Cancer 2007;121:1571-8.
35. Huncharek M, Muscat J, Kupelnick B. Dairy products, dietary calcium and vitamin D intake as risk factors for prostate cancer: a meta-analysis of 26,769 cases from 45 observational studies. Nutr Cancer 2008;60: 421-41.
36. Qin LQ, Xu JY, Wang PY, Kaneko T, Hoshi K, Sato A. Milk consumption is a risk factor for prostate cancer: meta-analysis of casecontrol studies. Nutr Cancer 2004;48:22-7.
37. Gao X, LaValley MP, Tucker KL. Prospective studies of dairy product and calcium intakes and prostate cancer risk: a meta-analysis. J Natl Cancer Inst 2005;97:1768-77.
38. Qin LQ, Xu JY, Wang PY, Tong J, Hoshi K. Milk consumption is a risk factor for prostate cancer in Western countries: evidence from cohort studies. Asia Pac J Clin Nutr 2007;16:467-76.
39. 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.
40. Snowdon DA, Phillips RL, Choi W. Diet, obesity, and risk of fatal prostate cancer. Am J Epidemiol 1984;120:244-50.
41. Severson RK, Nomura AM, Grove JS, Stemmermann GN. A prospective study of demographics, diet, and prostate cancer among men of Japanese ancestry in Hawaii. Cancer Res 1989;49:1857-60.
42. Mills PK, Beeson WL, Phillips RL, Fraser GE. Cohort study of diet, lifestyle, and prostate cancer in Adventist men. Cancer 1989;64:598-604.
43. Thompson MM, Garland C, Barrett-Connor E, Khaw KT, Friedlander NJ, Wingard DL. Heart disease risk factors, diabetes, and prostatic cancer in an adult community. Am J Epidemiol 1989;129:511-7.
44. Ursin G, Bjelke E, Heuch I, Vollset SE. Milk consumption and cancer incidence: a Norwegian prospective study. Br J Cancer 1990;61:454-9.
45. Hsing AW, McLaughlin JK, Schuman LM, Bjelke E, Gridley G, Wacholder S, Chien HT, Blot WJ. Diet, tobacco use, and fatal prostate cancer: results from the Lutheran Brotherhood Cohort Study. Cancer Res 1990;50:6836-40.
46. Le Marchand L, Kolonel LN, Wilkens LR, Myers BC, Hirohata T. Animal fat consumption and prostate cancer: a prospective study in Hawaii. Epidemiology 1994;5:276-82.
47. Grönberg H, Damber L, Damber JE. Total food consumption and body mass index in relation to prostate cancer risk: a case-control study in Sweden with prospectively collected exposure data. J Urol 1996;155:969-74.
48. Schuurman AG, van den Brandt PA, Dorant E, Goldbohm RA. Animal products, calcium and protein and prostate cancer risk in The Netherlands Cohort Study. Br J Cancer 1999;80:1107-13.
49. Chan JM, Stampfer MJ, Ma J, Gann PH, Gaziano JM, Giovannucci EL. Dairy products, calcium, and prostate cancer risk in the Physicians' Health Study. Am J Clin Nutr 2001;74:549-54.
50. Michaud DS, Augustsson K, Rimm EB, Stampfer MJ, Willet WC, Giovannucci E. A prospective study on intake of animal products and risk of prostate cancer. Cancer Causes Control 2001;12:557-67.
51. Berndt SI, Carter HB, Landis PK, Tucker KL, Hsieh LJ, Metter EJ, Platz EA. Calcium intake and prostate cancer risk in a long-term aging study: the Baltimore Longitudinal Study of Aging. Urology 2002;60: 1118-23.
52. Rodriguez C, Jacobs EJ, Patel AV, Calle EE, Feigelson HS, Fakhrabadi-Shokoohi D, Thun MJ. Jewish ethnicity and prostate cancer mortality in two large US cohorts. Cancer Causes Control 2002;13:271-7.
53. Rodriguez C, McCullough ML, Mondul AM, Jacobs EJ, Fakhrabadi-Shokoohi D, Giovannucci EL, Thun MJ, Calle EE. Calcium, dairy products, and risk of prostate cancer in a prospective cohort of United States men. Cancer Epidemiol Biomarkers Prev 2003;12:597-603.
54. Allen NE, Sauvaget C, Roddam AW, Appleby P, Nagano J, Suzuki G, Key TJ, Koyama K. A prospective study of diet and prostate cancer in Japanese men. Cancer Causes Control 2004;15:911-20.
55. Leitzmann MF, Stampfer MJ, Michaud DS, Augustsson K, Colditz GC, Willett WC, Giovannucci EL. Dietary intake of n-3 and n-6 fatty acids and the risk of prostate cancer. Am J Clin Nutr 2004;80:204-16.
56. Baron JA, Beach M, Wallace K, Grau MV, Sandler RS, Mandel JS, Heber D, Greenberg ER. Risk of prostate cancer in a randomized clinical trial of calcium supplementation. Cancer Epidemiol Biomarkers Prev 2005;14: 586-9.
57. Tseng M, Breslow RA, Graubard BI, Ziegler RG. Dairy, calcium, and vitamin D intakes and prostate cancer risk in the National Health and Nutrition Examination Epidemiologic Follow-up Study cohort. Am J Clin Nutr 2005;81:1147-54.
58. Chan JM, Holick CN, Leitzmann MF, Rimm EB,Willett WC, Stampfer MJ, Giovannucci EL. Diet after diagnosis and the risk of prostate cancer progression, recurrence, and death (United States). Cancer Causes Control 2006;17:199-208.
59. Wright ME, Bowen P, Virtamo J, Albanes D, Gann PH. Estimated phytanic acid intake and prostate cancer risk: a prospective cohort study. Int J Cancer 2012;131:1396-406.
60. Pettersson A, Kasperzyk JL, Kenfield SA, Richman EL, Chan JM, Willett WC, Stampfer MJ, Mucci LA, Giovannucci EL. Milk and dairy consumption among men with prostate cancer and risk of metastases and prostate cancer death. Cancer Epidemiol Biomarkers Prev 2012;21:428-36.
61. Giovannucci E, Rimm EB, Wolk A, Ascherio A, Stampfer MJ, Colditz GA, Willett WC. Calcium and fructose intake in relation to risk of prostate cancer. Cancer Res 1998;58:442-7.
62. Veierod MB, Laake P, Thelle DS. Dietary fat intake and risk of prostate cancer: a prospective study of 25,708 Norwegian men. Int J Cancer 1997;73:634-8.
63. Chan JM, Pietinen P, Virtanen M, Malila N, Tangrea J, Albanes D, Virtamo J. Diet and prostate cancer risk in a cohort of smokers, with a specific focus on calcium and phosphorus (Finland). Cancer Causes Control 2000;11:859-67.
64. DerSimonian R, Kacker R. Random-effects model for meta-analysis of clinical trials: an update. Contemp Clin Trials 2007;28:105-14.
65. 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.
66. US Department of Agriculture, Agricultural Research Service. 2006. Nutrient Data Laboratory Home Page [Internet]. USDA National Nutrient Database for Standard Reference, Release 19 [cited 2013 Apr 20]. Available from: http://www.ars.usda.gov/ba/bhnrc/ndl.
67. Royston P. A strategy for modelling the effect of a continuous covariate in medicine and epidemiology. Stat Med 2000;19:1831-47.
68. Higgins JP, Thompson SG. Quantifying heterogeneity in a metaanalysis. Stat Med 2002;21:1539-58.
69. Egger M, Davey SG, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997;315:629-34.
70. Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics 1994;50:1088-101.
71. Duval S, Tweedie R. Trim and fill: A simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics 2000;56:455-63.
72. Smit E, Garcia-Palmieri MR, Figueroa NR, McGee DL, Messina M, Freudenheim JL, Crespo CJ. Protein and legume intake and prostate cancer mortality in puerto rican men. Nutr Cancer 2007;58:146-52.
73. Giovannucci E. Dietary influences of 1,25(OH)2 vitamin D in relation to prostate cancer: a hypothesis. Cancer Causes Control 1998;9:567-82.
74. McCullough ML,Weinstein SJ, Freedman DM, Helzlsouer K, Flanders WD, Koenig K, Kolonel L, Laden F, Le Marchand L, Purdue M, et al. Correlates of circulating 25-hydroxyvitamin D: Cohort Consortium Vitamin D Pooling Project of Rarer Cancers. Am J Epidemiol 2010; 172:21-35.
75. Chen TC, Holick MF. Vitamin D and prostate cancer prevention and treatment. Trends Endocrinol Metab 2003;14:423-30.
76. Jones G, Strugnell SA, DeLuca HF. Current understanding of the molecular actions of vitamin D. Physiol Rev 1998;78:1193-231.
77. Gilbert R, Martin RM, Beynon R, Harris R, Savovic J, Zuccolo L, Bekkering GE, Fraser WD, Sterne JA, Metcalfe C. Associations of circulating and dietary vitamin D with prostate cancer risk: a systematic review and dose-response meta-analysis. Cancer Causes Control 2011;22:319-40.
78. Ma J, Giovannucci E, Pollak M, Chan JM, Gaziano JM, Willett WC, Stampfer MJ. Milk intake, circulating levels of insulin-like growth factor-I, and risk of colorectal cancer in men. J Natl Cancer Inst 2001; 93:1330-6.
79. Qin LQ, He K, Xu JY. Milk consumption and circulating insulin-like growth factor-I level: a systematic literature review. Int J Food Sci Nutr 2009;60(Suppl 7):330-40.
80. Allen NE, Appleby PN, Davey GK, Key TJ. Hormones and diet: low insulin-like growth factor-I but normal bioavailable androgens in vegan men. Br J Cancer 2000;83:95-7.
81. Cohen P, Peehl DM, Lamson G, Rosenfeld RG. Insulin-like growth factors (IGFs), IGF receptors, and IGF-binding proteins in primary cultures of prostate epithelial cells. J Clin Endocrinol Metab 1991;73:401-7.
82. Cohen P, Peehl DM, Rosenfeld RG. The IGF axis in the prostate. Horm Metab Res 1994;26:81-4.
83. Allen NE, Key TJ, Appleby PN, Travis RC, Roddam AW, Rinaldi S, Egevad L, Rohrmann S, Linseisen J, Pischon T. Serum insulin-like growth factor (IGF)-I and IGF-binding protein-3 concentrations and prostate cancer risk: results from the European Prospective Investigation into Cancer and Nutrition. Cancer Epidemiol Biomarkers Prev 2007;16: 1121-7.
84. Chan JM, Stampfer MJ, Giovannucci E, Gann PH, Ma J, Wilkinson P, Hennekens CH, Pollak M. Plasma insulin-like growth factor-I and prostate cancer risk: a prospective study. Science 1998;279:563-6.
85. Roddam AW, Allen NE, Appleby P, Key TJ, Ferrucci L, Carter HB, Metter EJ, Chen C, Weiss NS, Fitzpatrick A, et al. Insulin-like growth factors, their binding proteins, and prostate cancer risk: analysis of individual patient data from 12 prospective studies. Ann Intern Med 2008;149:461-71, W83-8.
86. Dagnelie PC, Schuurman AG, Goldbohm RA, van den Brandt PA. Diet, anthropometric measures and prostate cancer risk: a review of prospective cohort and intervention studies. BJU Int 2004;93:1139-50.