Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Article
  • Published:

Highly elevated PSA and dietary PhIP intake in a prospective clinic-based study among African Americans

Abstract

African-American men die from prostate cancer (PC) nearly twice as often as white US men and consume about twice as much of the predominant US dietary heterocyclic amine, 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP), a genotoxic rat-prostate carcinogen found primarily in well-cooked chicken and beef. To investigate the hypothesis that PhIP exposure increases PC risk, an ongoing prospective clinic-based study compared PC screening outcomes with survey-based estimates of dietary PhIP intake among 40–70-year-old African-American men with no prior PC in Oakland, CA. They completed food-frequency and meat-cooking/consumption questionnaires and had a prostate-specific antigen (PSA) test and digital-rectal exam. Results for 392 men indicated a 17 (±17) ng/kg day mean (±1 s.d.) daily intake of PhIP, about twice that of white US men of similar age. PhIP intake was attributable mostly to chicken (61%) and positively associated (R2=0.32, P<0.0001) with saturated fat intake. An odds ratio (95% confidence interval) of 31 (3.1–690) for highly elevated PSA 20 ng/ml was observed in the highest 15% vs lowest 50% of estimated daily PhIP intake (30 vs 10 ng/kg day) among men 50+ years old (P=0.0002 for trend) and remained significant after adjustment for self-reported family history of (brother or father) PC, saturated fat intake and total energy intake. PSA measures were higher in African-American men with positive family history (P=0.007 all men, P<0.0001 highest PSA quartile). These preliminary results are consistent with a positive association between PhIP intake and highly elevated PSA, supporting the hypothesis that dietary intervention may help reduce PC risk.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1

Similar content being viewed by others

Abbreviations

HA:

heterocyclic amine

PC:

prostate cancer

PhIP:

2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (105650-23-5)

References

  1. Thompson LH, Tucker JD, Stewart SA, Christensen ML, Salazar EP, Carrano AV et al. Genotoxicity of compounds from cooked beef in repair-deficient CHO cells versus salmonella mutagenicity. Mutagen 1987; 2: 483–487.

    Article  CAS  Google Scholar 

  2. Keating GA, Layton DW, Felton JS . Factors determining dietary intakes of heterocyclic amines in cooked foods. Mutat Res 1999; 443: 149–156.

    Article  CAS  PubMed  Google Scholar 

  3. Keating GA, Sinha R, Layton D, Salmon CP, Knize MG, Bogen KT et al. Comparison of heterocyclic amine levels in home-cooked meats with exposure indicators. Cancer Causes Control 2000; 11: 731–739.

    Article  CAS  PubMed  Google Scholar 

  4. Bogen KT . Cancer potencies of heterocyclic amines found in cooked foods. Food Chem Toxicol 1994; 32: 505–515.

    Article  CAS  PubMed  Google Scholar 

  5. Layton DW, Bogen KT, Knize MG, Hatch FT, Johnson VM, Felton J . Cancer risk assessment of heterocyclic amines in cooked foods: an analysis and implications for research. Carcinogenesis 1995; 16: 39–52.

    Article  CAS  PubMed  Google Scholar 

  6. Felton JS, Knize MG, Wood C, Wuebbles BJ, Healy SK, Stuermer DH et al. Isolation and characterization of new mutagens from fried ground beef. Carcinogenesis 1984; 5: 95–102.

    Article  CAS  PubMed  Google Scholar 

  7. Felton JS, Knize MG, Shen NH, Andresen BD, Bjeldanes LF, Hatch FT . Identification of the mutagens in cooked beef. Environ Health Perspect 1986; 67: 17–24.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Felton JS, Pais P, Salmon CP, Knize MG . Chemical analysis and significance of heterocyclic aromatic amines. Z Lebensm Unters Forsch A 1998; 207: 434–440.

    Article  CAS  Google Scholar 

  9. Felton JS, Knize MG . Heterocyclic-amine mutagens/carcinogens in foods. In: Cooper CS, Grover PL (eds). Handbook of Experimental Pharmacology, 94/1. Springer-Verlag: Berlin, 1990, pp 471–502.

    Google Scholar 

  10. Felton JS, Knize MG . New mutagens from cooked food. In: Pariza M, Aeschbacher H-U, Felton JS, Sato S (eds). Mutagens and Carcinogens in the Diet. Wiley-Liss Inc.: New York, 1990, pp 19–38.

    Google Scholar 

  11. Sinha R, Rothman N, Brown ED, Salmon CP, Knize MG, Swanson CA et al. High concentrations of the carcinogen 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine occur in chicken but are dependent on the cooking method. Cancer Res 1995; 55: 4516–4519.

    CAS  PubMed  Google Scholar 

  12. Esumi H, Ohgaki H, Kohzen E, Takayama S, Sugimura T . Induction of lymphoma in CDF1 mice by the food mutagen, 2-amino-1-methyl-6-phenylimidazo-[4,5-b]pyridine. Cancer Res 1989; 80: 1176–1178.

    CAS  Google Scholar 

  13. Ochiai M, Ogawa K, Wakabayashi K, Sugimura T, Nagase S, Esumi H et al. Induction of intestinal adenocarcinomas by 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine in Nagase analbuminemic rats. Jap J Cancer Res (Gann) 1991; 82: 363–366.

    Article  CAS  Google Scholar 

  14. Ohgaki H, Takayama S, Sugimura T . Carginogenicity of heterocyclic amines in cooked foods. Mutat Res 1991; 259: 339–410.

    Article  Google Scholar 

  15. Ito N, Hasegawa R, Imaida K, Tamano S, Hagiwara A, Hirose M et al. Carcinogenicity of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) in the rat. Mutat Res 1997; 376: 107–114.

    Article  CAS  PubMed  Google Scholar 

  16. Ito N, Hasegawa R, Sano M, Tamano S, Esumi H, Takayama S et al. A new colon and mammary carcinogen in cooked food, 2-amino-1-methyl-6-phenylimidazo-[4,5-b]pyridine (PhlP). Carcinogenesis 1991; 12: 1503–1506.

    Article  CAS  PubMed  Google Scholar 

  17. Hasegawa R, Sano M, Tamano S, Imaida K, Shirai T, Nagao M et al. Carcinogenicity of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) in the rat. Carcinogenesis 1993; 14: 2523–2557.

    Article  Google Scholar 

  18. Ghoshal A, Preisegger K-H, Takayama T, Thorgeirsson S, Snyderwine EG . Induction of mammary tumors in female Sprague–Dawley rats by the food-derived carcinogen 2-amino-1-methyl-6-phenylimidazo[4, 5,-b]pyridine and effect of dietary fat. Carcinogenesis 1994; 15: 2429–2433.

    Article  CAS  PubMed  Google Scholar 

  19. Shirai T, Sano M, Tamano S, Takahashi S, Hirose M, Futakushi M et al. The prostate: a target for carcinogenicity of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) derived from cooked foods. Cancer Res 1997; 57: 195–198.

    CAS  PubMed  Google Scholar 

  20. Shirai T, Cui L, Takahashi S, Futakuchi M, Asamoto M, Kato K et al. Carcinogenicity of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) in the rat prostate and induction of invasive carcinomas by subsequent treatment with testosterone propionate. Cancer Lett 1999; 143: 217–221.

    Article  CAS  PubMed  Google Scholar 

  21. Gooderham NJ, Zhu H, Lauber S, Boyce A, Creton S . Molecular and genetic toxicology of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP). Mutat Res 2002; 506–507: 91–99.

    Article  PubMed  Google Scholar 

  22. U.S. Department of Health and Human Services (USDHHS). Final Report on Carcinogens Background Document for Selected Heterocyclic Amines: PhIP, MeIQ, and MeIQx. September 12, 2002. Prepared by the Technology Planning and Management Corp for the USDHHS National Toxicology Program, Research Triangle Park, NC. ntp.neihs.nih.gov/ntp/newhomeroc/roc11/HCAsPub.pdf: 2002.

  23. Thorgeirsson SS . Metabolic determinants in the carcinogenicity of aromatic amines. In: Greim H, Jung R, Kramer M, Marquardt H, Oesch F (eds). Biochemical Basis of Chemical Carcinogenesis. Raven Press: New York, NY, 1984, pp 47–56.

    Google Scholar 

  24. Thorgeirsson SS, Glowinski IB, McManus ME . Metabolism, mutagenicity and carcinogenicity of aromatic amines. In: Hodgson E, Bend JR, Philpot RM (eds). Reviews in Biochemical Toxicology 5. Elsevier Biomedical: New York, Amsterdam, Oxford, 1983, pp 349–386.

    Google Scholar 

  25. Rosenkranz HS, Mermeistein R . The genotoxicity, metabolism and carcinogenicity of nitrated polycyclic aromatic hydrocarbons. J Environ Sci Health 1985; C3: 221–272.

    CAS  Google Scholar 

  26. Sato S, Negishi C, Umemoto A, Sugimura T . Metabolic aspects of pyrolysis mutagens in food. Environ Health Perspect 1986; 67: 105–109.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Kato R, Yamazoe Y . Metabolic activation and covalent binding to nucleic acids of carcinogenic heterocyclic amines from cooked food and amino acid pyrolysates. Jap J Cancer Res (Gann) 1987; 81: 10–14.

    Google Scholar 

  28. Snyderwine EG, Battula N . Selective mutagenic activation by cytochrome P3-450 of carcinogenic arylamines found in foods. J Natl Cancer Inst 1989; 81: 223–227.

    Article  CAS  PubMed  Google Scholar 

  29. McManus ME, Burgess WM, Veronese ME, Hugget A, Quattrochi LC, Tukey RH . Metabolism of 2-acetylaminofluorene and benzo(a)pyrene and activation of food-derived heterocyclic amine mutagens by cytochromes P450. Cancer Res 1990; 50: 3367–3376.

    CAS  PubMed  Google Scholar 

  30. Turesky RJ, Lang NP, Butler MA, Teitel CH, Kadlubar FF . Metabolic activation of carcingenic heterocyclic aromatic amines by human liver and colon. Carcinogenesis 1991; 12: 1839–1845.

    Article  CAS  PubMed  Google Scholar 

  31. Davis CD, Schut HAJ, Adamson RH, Thorgeirsson UP, Thorgeirsson SS, Snyderwine EG . Mutagenic activation of IQ, PhlP and MelQx by hepatic microsomes from rat, monkey and man: low mutagenic activation of MelQx in cynomolgous monkeys in vitro reflects low DNA adduct levels in vivo. Carcinogenesis 1993; 14: 61–65.

    Article  CAS  PubMed  Google Scholar 

  32. Kaderlik KR, Minchin RF, Mulder GJ, Ilett KF, Daugaard-Jenson M, Teitel CH et al. Metabolic activation pathway for the formation of DNA adducts of the carcinogen 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) in rat extrahepatic tissues. Carcinogenesis 1994; 15: 1703–1709.

    Article  CAS  PubMed  Google Scholar 

  33. Kaderlik KR, Mulder GJ, Shaddock JG, Casciano DA, Teitel CH, Kadlubar FF . Effect of glutathione depletion and inhibition of glucuronidation and sulfation on 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) metabolism, PhIP–DNA adduct formation and unscheduled DNA synthesis in primary rat hepatocytes. Carcinogenesis 1994; 15: 1711–1716.

    Article  CAS  PubMed  Google Scholar 

  34. Takahashi S, Tamano S, Hirose M, Kimoto N, Ikeda Y, Sakakibara M et al. Immunohistochemical demonstration of carcinogen–DNA adducts in tissues of rats given 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP): detection in paraffin-embedded sections and tissue distribution. Cancer Res 1998; 58: 4307–4313.

    CAS  PubMed  Google Scholar 

  35. Schut HAJ, Snyderwine EG . DNA adducts of heterocyclic amine food mutagens: implications for mutagenesis and carcinogenesis. Carcinogenesis 1999; 20: 353–368.

    Article  CAS  PubMed  Google Scholar 

  36. Stuart GR, Holcroft J, de Boer JG, Glickman BW . Prostate mutations in rats induced by suspected human carcinogen 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP). Cancer Res 2000; 60: 266–268.

    CAS  PubMed  Google Scholar 

  37. Williams JA, Martin FL, Muir GH, Hewer A, Grover PL, Phillips DH et al. Metabolic activation of carcinogens and expression of various cytochromes P450 in human prostate tissue. Carcinogenesis 2000; 21: 1683–1689.

    Article  CAS  PubMed  Google Scholar 

  38. Lawson T, Kolar C . Human prostate epithelial cells metabolize chemicals of dietary origin to mutagens. Cancer Lett 2002; 175: 141–146.

    Article  CAS  PubMed  Google Scholar 

  39. Martin FL, Cole KJ, Muir GH, Kooiman GG, Williams JA, Sherwood RA et al. Primary cultures of prostate cells and their ability to activate carcinogens. Prostate Cancer Prostatic Dis 2002; 5: 96–104.

    Article  CAS  PubMed  Google Scholar 

  40. Di Paolo OA, Teitel CH, Nowell S, Coles BF, Kadlubar FF . Expression of cytochromes P450 and glutathione S-transferases in human prostate, and the potential for activation of heterocyclic amine carcinogens via acetyle-CoA-, PAPS- and ATP-dependent pathways. Int J Cancer 2005; 117: 8–13.

    Article  CAS  PubMed  Google Scholar 

  41. Lauber SN, Ali S, Gooderham NJ . The cooked food derived carcinogen 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine is a potent oestrogen: a mechanistic basis for its tissue-specific carcinogenicity. Carcinogenesis 2004; 25: 2509–2517.

    Article  CAS  PubMed  Google Scholar 

  42. Miller BA, Kolonel LN, Bernstein L, Young Jr JL, Swanson GM, West D et al. (eds). Racial/Ethic Patterns of Cancer in the United States 1988–1992, NIH Pub. No. 96-4104. National Cancer Institute: Bethesda, MD, 1996.

    Google Scholar 

  43. Robbins AS, Whittemore AS, Van Den Eden SK . Race, prostate cancer survival, and membership in a large health maintenance organization. J Natl Cancer Inst 1998; 90: 986–990.

    Article  CAS  PubMed  Google Scholar 

  44. Hsing AW, Tsao L, Devesa SS . International trends and patterns of prostate cancer incidence and mortality. Int J Cancer 2000; 85: 60–67.

    Article  CAS  PubMed  Google Scholar 

  45. Schurrman AG, Zeegers PA, Goldbohm RA, van den Brandt PA . A case–control study on prostate cancer risk in relation to family history of prostate cancer. Epidemiology 1999; 10: 192–195.

    Article  Google Scholar 

  46. Hemminki K, Czene K . Age specific and attributable risks of familial prostate carcinoma from the family-cancer database. Cancer 2002; 95: 1346–1353.

    Article  PubMed  Google Scholar 

  47. Zeegers MP, Jellema A, Ostrer H . Empiric risk of prostate carcinoma for relatives of patients with prostate carcinoma: a meta-analysis. Cancer 2003; 97: 1894–1903.

    Article  PubMed  Google Scholar 

  48. Hemminki K, Chen B . Familial association of prostate cancer with other cancers in the Swedish Family-Center Database. Prostate 2005; 65: 188–194.

    Article  PubMed  Google Scholar 

  49. Tomlins SA, Rhodes DR, Perner S, Dhanasekaran M, Mehra R, Sun X-W et al. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science 2005; 310: 644–648.

    Article  CAS  PubMed  Google Scholar 

  50. Hsing AW . Hormones and prostate cancer: what's next? Epidemiol Rev 2001; 23: 42–58.

    Article  CAS  PubMed  Google Scholar 

  51. Pettaway CA . Racial differences in the adrogen/androgen receptor pathway in prostate cancer. J Natl Med Assoc 1999; 91: 652–660.

    Google Scholar 

  52. Ross RK, Pike MC, Coetzee GA, Reichhardt JKV, Yu MC, Feigelson H et al. Androgen metabolism and prostate cancer: establishing a model of genetic susceptibility. Cancer Res 1998; 58: 4497–4504.

    CAS  PubMed  Google Scholar 

  53. Minami Y, Staples MP, Giles GG . The incidence of colon, breast and prostate cancer in Italian migrants to Victoria, Australia. Eur J Cancer 1993; 29A: 1735–1740.

    Article  CAS  PubMed  Google Scholar 

  54. Mettlin C . Recent developments in the epidemiology of prostate cancer. Eur J Cancer 1997; 33: 340–347.

    Article  CAS  PubMed  Google Scholar 

  55. Angwafo FF . Migration and prostate cancer: an international perspective. J Natl Med Assoc 1998; 90 (11 Suppl): S720–S723.

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Whittemore AS, Kolonel LN, Wu AH, John EM, Gallager RP, Howe GR et al. Prostate cancer in relation to diet, physical activity, and body size in Blacks, Whites, and Asians in the United States and Canada. J Natl Cancer Inst 1995; 87: 652–661.

    Article  CAS  PubMed  Google Scholar 

  57. Kolonel LN, Nomura AMY, Cooney RV . Dietary fat and prostate cancer: current status. J Natl Cancer Inst 1999; 91: 414–428.

    Article  CAS  PubMed  Google Scholar 

  58. Hayes RB, Ziegler RG, Gridley G, Swanson C, Greenberg RS, Swanson GM et al. Dietary factors and risks for prostate cancer among blacks and whites in the United States. Cancer Epidemiol Biomark Prev 1999; 8: 25–34.

    CAS  Google Scholar 

  59. Daniels LK, Snetselaar LG, Smith BJ, Stewart RE, Robbins MEC . Problems with the assessment of dietary fat in prostate cancer studies. Am J Epidemiol 2004; 160: 436–444.

    Article  Google Scholar 

  60. Giovannucci E, Rimm EB, Stampfer MJ, Colditz GA, Willett WC . Height, body weight, and risk of prostate cancer. Cancer Epidemiol Biomark Prevent 1997; 6: 557–563.

    CAS  Google Scholar 

  61. Giovannucci E, Rimm EB, Wolk A, Ascherio A, Stampfer MJ, Colditz GA et al. Calcium and fructose intake in relation to risk of prostate cancer. Cancer Res 1998; 58: 442–447.

    CAS  PubMed  Google Scholar 

  62. Cohen JH, Kristal AR, Stanford JL . Fruit and vegetable intakes and prostate cancer. J Natl Cancer Inst 2000; 92: 61–68.

    Article  CAS  PubMed  Google Scholar 

  63. Chan J, Giovannucci E . Vegetables, fruits, associated micronutrients, and risk of prostate cancer. Epidemiol Rev 2001; 23: 82–86.

    Article  CAS  PubMed  Google Scholar 

  64. Chan J, Giovannucci E . Dairy products, calcium, and vitamin D, and risk of prostate cancer. Epidemiol Rev 2001; 23: 87–92.

    Article  CAS  PubMed  Google Scholar 

  65. Kristal AR, Lampe JW . Brassica vegetables and prostate cancer risk: a review of the epidemiological evidence. Nutr Cancer 2002; 42: 1–9.

    Article  PubMed  Google Scholar 

  66. Bodiwala D, Luscombe CJ, Liu S, Saxby M, French M, Jones PW et al. Cancer potencies of heterocyclic amines found in cooked foods. Cancer Lett 2003; 192: 145–149.

    Article  CAS  PubMed  Google Scholar 

  67. U.S. Department of Agriculture (USDA). 1994–96 Continuing Survey of Food Intakes by Individuals and 1994–96 Diet and Health Knowledge Survey (CSFII/DHKS 1994–96 Data Set). CD-ROM. USDA Agricultural Research Service, Beltsville Human Nutrition Research Center, Food Surveys Research Group: Beltsville, MD, 1998.

  68. Mills PK, Beeson WL, Phillips RL, Fraser GE . Cohort of diet, lifestyle and prostate cancer in Adventist men. Cancer 1989; 64: 598–604.

    Article  CAS  PubMed  Google Scholar 

  69. Shiffman MH, Felton JS . Re ‘Fried foods and the risk of colon cancer’. Am J Epidemiol 1990; 131: 376–378.

    Article  Google Scholar 

  70. Gerhardsson de Verdier M, Hagman U, Peters RK, Steineck G, Õvervik E . Meat, cooking methods and colorectal cancer: a case-referent study in Stockholm. Int J Cancer 1991; 49: 520–525.

    Article  CAS  PubMed  Google Scholar 

  71. Talamini R, Franceschi S, La Vecchia C, Serraino D, Negri E . Diet and prostatic cancer: a case–control study in northern Italy. Nutr Cancer 1992; 18: 277–286.

    Article  CAS  PubMed  Google Scholar 

  72. Lang NP, Butler MA, Massengill J, Lawson M, Stotts RC, Hauer-Hensen M et al. Rapid metabolic phenotypes for acetyltransferase and cytochrome P4501A2 and putative exposure to food-borne heterocyclic amines increase the risk for colorectal cancer or polyps. Cancer Epidemiol Biomark Prev 1994; 8: 675–682.

    Google Scholar 

  73. De Stefani E, Fierro L, Barrios E, Ronco A . Tobacco, alcohol, diet and risk of prostate cancer. Tumori 1995; 81: 315–320.

    Article  CAS  PubMed  Google Scholar 

  74. Ewings P, Bowie C . A case–control study of cancer of the prostate in Somerset and east Devon. Br J Cancer 1996; 74: 661–666.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Probst-Hensch NM, Sinha R, Longnecker MP, Witte JS, Ingles SA, Frankl HD et al. Meat preparation and colorectal adenomas in a large sigmoidoscopy-based case–control study in California (United States). Cancer Causes Control 1997; 8: 175–183.

    Article  CAS  PubMed  Google Scholar 

  76. Ward MH, Sinha R, Heinman EF, Rothman N, Markin R, Weisenburger DD et al. Risk of adenocarcinoma of the stomach and esophagus with meat cooking method and doneness preference. Int J Cancer 1997; 71: 14–19.

    Article  CAS  PubMed  Google Scholar 

  77. Kampman E, Slattery ML, Bigler J, Leppert M, Samowitz W, Caan BJ et al. Meat consumption, genetic susceptibility, and colon cancer risk: a United States multicenter case–control study. Cancer Epidemiol Biomark Prev 1999; 8: 15–24.

    CAS  Google Scholar 

  78. Norrish AE, Ferguson LR, Knize MG, Felton JS, Sharpe SJ, Jackson RT . Heterocyclic amine content of cooked meat and risk of prostate cancer. J Natl Cancer Inst 1999; 91: 2038–2044.

    Article  CAS  PubMed  Google Scholar 

  79. Sinha R, Kulldorff M, Curtin J, Brown CC, Alavanja MC, Swanson C . Fried, well-done red meat and risk of lung cancer in women (United States). Cancer Causes Control 1998; 9: 621–630.

    Article  CAS  PubMed  Google Scholar 

  80. Sinha R, Chow WH, Kulldorff M, Denobile J, Butler J, Garcia-Closas M et al. Well-done, grilled red meat increases the risk of colorectal adenomas. Cancer Res 1999; 59: 4320–4324.

    CAS  PubMed  Google Scholar 

  81. Zheng W, Gustafson DR, Sinha R, Cerhan JR, Moore D, Hong CP et al. Well-done meat intake and the risk of breast cancer. J Natl Cancer Inst 1998; 90: 1724–1729.

    Article  CAS  PubMed  Google Scholar 

  82. Sinha R, Rothman N . Role of well-done, grilled red meat, heterocyclic amines (HCAs) in the etiology of human cancer. Cancer Lett 1999; 143: 189–194.

    Article  CAS  PubMed  Google Scholar 

  83. Zheng W, Deitz AC, Campbell DR, Wen WQ, Cerhan JR, Sellers TA et al. N-acetyltransferase 1 genetic polymorphism, cigarette smoking, well-done meat intake, and breast cancer risk. Cancer Epidemiol Biomark Prev 1999; 8: 233–239.

    CAS  Google Scholar 

  84. Sinha R . An epidemiological approach to studying heterocyclic amines. Mutat Res 2002; 506/507: 197–204.

    Article  Google Scholar 

  85. Butler LM, Sinha R, Millikan RC, Martin CF, Newman B, Gammon MD et al. Heterocyclic amines, meat intake, and association with colon cancer in a population-based study. Am J Epidemiol 2003; 157: 434–445.

    Article  CAS  PubMed  Google Scholar 

  86. Chen K, Liang JQ, Zhang Y, Wan YZ . Meta-analysis of risk factors for colorectal cancer. World J Gastroenterol 2003; 9: 1598–1600.

    Article  PubMed  PubMed Central  Google Scholar 

  87. Murtaugh MA, Ma K, Sweeney C, Caan BJ Slattery ML . Meat consumption patterns and preparation, genetic variants of metabolic enzymes, and their association with rectal cancer in men and women. J Nutr 2004; 134: 776–784.

    Article  CAS  PubMed  Google Scholar 

  88. Chao A, Thun MJ, Connell CJ, McCullough ML, Jacobs EJ, Flanders WD et al. Meat consumption and risk of colorectal cancer. JAMA 2005; 293: 233–234.

    Article  Google Scholar 

  89. Rodriguez C, McCullough ML, Mondul AM, Jacobs EJ, Chao A, Patel AV et al. Meat consumption among black and white men and risk of prostate cancer in the Cancer Prevention Study II Nutrition Cohort. Cancer Epidemiol Biomark Prev 2006; 15: 211–216.

    Article  Google Scholar 

  90. Sadri GH, Mahjub M . Meat consumption is a risk factor for colorectal cancer: meta-analysis of case–control studies. Pakistani J Nutr 2006; 5: 230–233.

    Article  Google Scholar 

  91. Lyon JL, Mahoney AW . Fried foods and the risk of colon cancer. Am J Epidemiol 1988; 128: 1000–1006.

    Article  CAS  PubMed  Google Scholar 

  92. Muscat JE, Wynder EL . The consumption of well-done red meat and the risk of colorectal cancer. Am J Public Health 1994; 84: 856–858.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Augustsson K, Skog K, Jagerstad M, Dickman PW, Steineck G . Dietary heterocyclic amines and cancer of the colon, rectum, bladder, and kidney: a population based study. Lancet 1999; 353: 703–707.

    Article  CAS  PubMed  Google Scholar 

  94. Delfino RJ, Sinha R, Smith C, West J, White E, Lin HJ et al. Breast cancer, heterocyclic aromatic amines from meat and N-acetyltransferase 2 genotype. Carcinogenesis 2000; 21: 607–615.

    Article  CAS  PubMed  Google Scholar 

  95. Carter HB, Pearson JD, Metter EJ, Brant LJ, Chan DW, Andres R et al. Longitudinal evaluation of prostrate-specific antigen levels in men with and without prostrate disease. J Am Med Assoc 1992; 267: 2215–2220.

    Article  CAS  Google Scholar 

  96. Oesterling JE, Jacobsen SJ, Chute CG, Guess HA, Girman CJ, Panser LA et al. Serum prostate-specific antigen in a community-based population of healthy men. J Am Med Assoc 1993; 270: 860–864.

    Article  CAS  Google Scholar 

  97. Etzioni R, Cha R, Cowen M . Serial prostate specific antigen screening for prostate cancer: a computer model evaluates competing strategies. J Urol 1999; 162: 741–748.

    Article  CAS  PubMed  Google Scholar 

  98. Abdalla I, Ray P, Vijayakumar S . Race and serum prostate-specific antigen levels: current status and future directions. Semin Urol Oncol 1998a; 16: 207–213.

    CAS  PubMed  Google Scholar 

  99. Abdalla I, Ray P, Ray V, Vaida F, Vijayakumar S . Comparison of serum prostate-specific antigen levels and PSA density in African American, white, and Hispanic men without prostate cancer. Urology 1998b; 51: 300–305.

    Article  CAS  PubMed  Google Scholar 

  100. Vijayakumar S, Winter K, Sause W, Gallagher MJ, Michalski J, Roach M et al. Prostate-specific antigen levels are higher in African-American than in white patients in a multicenter registration study: results of RTOG 94-12. Int J Radiat Oncol Biol Biophys 1998; 40: 17–25.

    Article  CAS  Google Scholar 

  101. Fowler Jr JE, Bigler SA, Kilambi NK, Land SA . Relationships between prostate-specific antigen and prostate volume in black and white men with benign prostate biopsies. Urology 1999; 53: 1175–1178.

    Article  PubMed  Google Scholar 

  102. Määttänen L, Auvinen A, Stenman U-H, Tammela T, Rannikko S, Aro J et al. Three-year results of the Finnish Prostate Cancer Screening Trial. J Natl Cancer Inst 2001; 93: 552–553.

    Article  PubMed  Google Scholar 

  103. Gerstenbluth RE, Seftel AD, Hampel N, Oefelein MG, Resnick MI . The accuracy of the increased prostate specific antigen level (greater than or equal to 20 ng/ml.) in predicting prostate cancer: is biopsy always required? J Urol 2002; 168: 1990–1993.

    Article  CAS  PubMed  Google Scholar 

  104. Smith RP, Malkowicz SB, Whittington R, VanArsdalen K, Tochner Z, Wein AJ . Identification of clinically significant prostate cancer by prostate-specific antigen screening. Arch Intern Med 2004; 164: 1227–1230.

    Article  PubMed  Google Scholar 

  105. Vollmer RT . Predictive probability of serum prostate-specific antigen for prostate cancer: an approach using Bayes rule. Clin Chem 2006; 125: 336–342.

    Google Scholar 

  106. Thompson IM, Pauler DK, Goodman PJ, Tangen CM, Lucia MS, Parnes HL et al. Prevalence of prostate cancer among men with a prostate-specific antigen level &lt;or=4.0 ng per milliliter. N Engl J Med 2004; 350: 2239–2246.

    Article  CAS  PubMed  Google Scholar 

  107. American Cancer Society (ACS). California Cancer Facts and Figures, 2006. ACS California Division and Public Health Institute California Cancer Registry: Oakland, CA, 2005.

  108. US Census Bureau. State and County QuickFacts (http://quickfacts.census.gov/qfd/states/06000.html, revised 8 June 2006); and American FactFinder, 2005 American Community Survey, custom tables B12002B, B01002B, B20017B (http://factfinder.census.gov): 2006.

  109. Block G, Hartman AM, Dresser CM, Carroll MD, Gannon J, Gardner L . A data-based approach to diet questionnaire design and testing. Am J Epidemiol 1986; 124: 453–469.

    Article  CAS  PubMed  Google Scholar 

  110. Sinha R, Rothman N, Salmon CP, Knize MG, Brown ED, Swanson CA et al. Heterocyclic amine content in beef cooked by different methods and to varying degrees of doneness and gravy made from meat drippings. Food Chem Toxicol 1998; 36: 279–287.

    Article  CAS  PubMed  Google Scholar 

  111. Sinha R, Knize MG, Salmon CP, Brown ED, Rhodes D, Felton JS et al. Heterocyclic amine content of pork products cooked by different methods and to varying degrees of doneness. Food Chem Toxicol 1998; 36: 289–297.

    Article  CAS  PubMed  Google Scholar 

  112. Cantwell M, Mittl B, Curtin J, Carrol R, Potischman N, Caporaso N et al. Relative validity of a food frequency questionnaire with a meat-cooking and heterocyclic amine module. Cancer Epidemiol Biomark Prev 2004; 13: 293–298.

    Article  CAS  Google Scholar 

  113. Bogen KT, Keating GA . US dietary exposures to heterocyclic amines. J Exposure Anal Environ Epidemiol 2001; 11: 155–168.

    Article  CAS  Google Scholar 

  114. Keating GA, Bogen KT . Methods to estimate heterocyclic amine concentrations in cooked meats in the U.S. diet. Food Chem Toxicol 2001; 39: 29–43.

    Article  CAS  PubMed  Google Scholar 

  115. Keating GA, Bogen KT . Estimates of heterocyclic amine intake in the U.S. population. J Chromatogr B 2004; 802: 127–133.

    Article  CAS  Google Scholar 

  116. Draper NR, Smith H . Applied Regression Analysis, 2nd edn. John Wiley & Sons: New York, NY, 1981.

    Google Scholar 

  117. Selvin S . Practical Biostatistical Methods. Duxbury Press: New York, NY, 1995.

    Google Scholar 

  118. Kendall M, Stuart A . The Advanced Theory of Statistics, vol. 2. MacMillan Publishing Co.: New York, NY, 1979, pp 159–160.

    Google Scholar 

  119. Breslow NE, Day NE . Statistical Methods in Cancer Research, Volume II – The Design and Analysis of Cohort Studies, IARC Scientific Publ. No. 82. International Agency for Cancer research (IARC): Lyon, France, 1987, pp 106–118.

    Google Scholar 

  120. Wolfram S . Mathematica Book, 4th edn. Cambridge University Press: Cambridge, UK, 1999.

    Google Scholar 

  121. Kidd LR, Stillwell WG, Yu MC, Wishnok JS, Skipper PL, Ross RK et al. Urinary excretion of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) in White, African American, and Asian-American men in Los Angeles County. Cancer Epidemiol Biomark Prev 1999; 8: 439–445.

    CAS  Google Scholar 

  122. Malfatti MA, Kulp KS, Knize MG, Davis C, Massengill JP, Williams S et al. The identification of [2-14C]2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine metabolites in humans. Carcinogenesis 1999; 20: 705–713.

    Article  CAS  PubMed  Google Scholar 

  123. U.S. Department of Agriculture (USDA). 1989–91 Continuing Survey of Food Intakes by Individuals and 1989–91 Diet and Health Knowledge Survey (CSFII/DHKS 1989–91 Data Set). CD-ROM. USDA Agricultural Research Service, Beltsville Human Nutrition Research Center, Food Surveys Research Group: Beltsville, MD, 1993.

  124. Zelterman D . Models for Discrete Data. Clarendon Press: Oxford, UK, 1999, pp 6–24.

    Google Scholar 

  125. Wilkens LR, Hankin JH, Yoshizawa CN, Kolonel LN, Lee J . Comparison of long-term dietary recall between cancer cases and noncases. Am J Epidemiol 1992; 136: 825–835.

    Article  CAS  PubMed  Google Scholar 

  126. Stark A . An historical review of the Harvard and the National Cancer Institute Food Frequency Questionnaires: their similarities, differences, and their limitations in assessment of food intake. Ecol Food Nutr 2002; 41: 35–74.

    Article  Google Scholar 

  127. Subar AF, Thompson FE, Kipnis V, Midthune D, Hurwitz P, McNutt S et al. Comparative validation of the Block, Willett, and National Cancer Institute food frequency questionnaires – The eating at America's table study. Am J Epidemiol 2001; 154: 1089–1099.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We appreciate comments on the earlier drafts of this manuscript (Jim Felton and Mark Knize, LLNL; Jennifer Kristiansen, UCSF; an anonymous reviewer) and for interview coordination (Kristiansen). This work was performed under the auspices of the US Department of Energy by University of California, Lawrence Livermore National Laboratory under Contract W-7405-Eng-48, with support by the National Cancer Institute (NIH Grant No. P01 CA55861-01) and the Department of Defense Prostate Cancer Research Program (award no. W81XWH-05-1-0153). Views and opinions of and endorsements by the author(s) do not reflect those of the US Army or the Department of Defense.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to K T Bogen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bogen, K., Keating, G., Chan, J. et al. Highly elevated PSA and dietary PhIP intake in a prospective clinic-based study among African Americans. Prostate Cancer Prostatic Dis 10, 261–269 (2007). https://doi.org/10.1038/sj.pcan.4500941

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/sj.pcan.4500941

Keywords

This article is cited by

Search

Quick links