, Volume 11, Issue 2–3, pp 205–220 | Cite as

The Causes and Prevention of Cancer: The Role of Environment

  • Bruce N. Ames
  • Lois Swirsky Gold


The idea that synthetic chemicals such as DDT are major contributors to human cancer has been inspired, in part, by Rachel Carson's passionate book, Silent Spring. This chapter discusses evidence showing why this is not true. We also review research on the causes of cancer, and show why much cancer is preventable.

Epidemiological evidence indicates several factors likely to have a major effect on reducing rates of cancer: reduction of smoking, increased consumption of fruits and vegetables, and control of infections. Other factors are avoidance of intense sun exposure, increases in physical activity, and reduction of alcohol consumption and possibly red meat. Already, risks of many forms of cancer can be reduced and the potential for further reductions is great. If lung cancer (which is primarily due to smoking) is excluded, cancer death rates are decreasing in the United States for all other cancers combined.

Pollution appears to account for less than 1% of human cancer; yet public concern and resource allocation for chemical pollution are very high, in good part because of the use of animal cancer tests in cancer risk assessment. Animal cancer tests, which are done at the maximum tolerated dose (MTD), are being misinterpreted to mean that low doses of synthetic chemicals and industrial pollutants are relevant to human cancer. About half of the chemicals tested, whether synthetic or natural, are carcinogenic to rodents at these high doses. A plausible explanation for the high frequency of positive results is that testing at the MTD frequently can cause chronic cell killing and consequent cell replacement, a risk factor for cancer that can be limited to high doses. Ignoring this greatly exaggerates risks. Scientists must determine mechanisms of carcinogenesis for each substance and revise acceptable dose levels as understanding advances.

The vast bulk of chemicals ingested by humans is natural. For example, 99.99% of the pesticides we eat are naturally present in plants to ward off insects and other predators. Half of these natural pesticides tested at the MTD are rodent carcinogens. Reducing exposure to the 0.01% that are synthetic will not reduce cancer rates. On the contrary, although fruits and vegetables contain a wide variety of naturally-occurring chemicals that are rodent carcinogens, inadequate consumption of fruits and vegetables doubles the human cancer risk for most types of cancer. Making them more expensive by reducing synthetic pesticide use will increase cancer. Humans also ingest large numbers of natural chemicals from cooking food. Over a thousand chemicals have been reported in roasted coffee: more than half of those tested (19/28) are rodent carcinogens. There are more rodent carcinogens in a single cup of coffee than potentially carcinogenic pesticide residues in the average American diet in a year, and there are still a thousand chemicals left to test in roasted coffee. This does not mean that coffee is dangerous but rather that animal cancer tests and worst-case risk assessment, build in enormous safety factors and should not be considered true risks.

The reason humans can eat the tremendous variety of natural chemical "rodent carcinogens" is that humans, like other animals, are extremely well protected by many general defense enzymes, most of which are inducible (i.e., whenever a defense enzyme is in use, more of it is made). Since the defense enzymes are equally effective against natural and synthetic chemicals one does not expect, nor does one find, a general difference between synthetic and natural chemicals in ability to cause cancer in high-dose rodent tests.

The idea that there is an epidemic of human cancer caused by synthetic industrial chemicals is false. In addition, there is a steady rise in life expectancy in the developed countries. Linear extrapolation from the maximum tolerated dose in rodents to low level exposure in humans has led to grossly exaggerated mortality forecasts.

Such extrapolations can not be verified by epidemiology. Furthermore, relying on such extrapolations for synthetic chemicals while ignoring the enormous natural background, leads to an imbalanced perception of hazard and allocation of resources. It is the progress of scientific research and technology that will continue to lengthen human life expectancy.

Zero exposure to rodent carcinogens cannot be achieved. Low levels of rodent carcinogens of natural origin are ubiquitous in the environment. It is thus impossible to obtain conditions totally free of exposure to rodent carcinogens or to background radiation. Major advances in analytical techniques enable the detection of extremely low concentrations of all substances, whether natural or synthetic, often thousands of times lower than could be detected 30 years ago.

Risks compete with risks: society must distinguish between significant and trivial risks. Regulating trivial risks or exposure to substances erroneously inferred to cause cancer at low-doses, can harm health by diverting resources from programs that could be effective in protecting the health of the public. Moreover, wealth creates health: poor people have shorter life expectancy than wealthy people. When money and resources are wasted on trivial problems, society's wealth and hence health is harmed.


Maximum Tolerate Dose Synthetic Chemical Defense Enzyme Cancer Risk Assessment Roasted Coffee 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Miller BA, Ries LAG, Hankey BF, Kosary CL, Harras A, Devesa SS, Edwards BK. SEER Cancer Statistics Review: 1973–1990, National Cancer Institute, NIH Pub. No. 93–2789, 1993.Google Scholar
  2. 2.
    Brown LM, Everett GD, Gibson R, Burmeister LF, Schuman LM, Blair A. Smoking and risk of non-Hodgkin's lymphoma and multiple myeloma, Cancer Causes Control, 1992; 3: 49–55.Google Scholar
  3. 3.
    Linet MS, McLaughlin JK, Hsing AW, Wacholder S, Co Chien HT, Schuman LM, Bjelke E, Blot WJ. Is cigarette smoking a risk factor for non-Hodgkin's lymphoma or multiple myeloma? Results from the Lutheran Brotherhood Cohort Study, Leukemia Res, 1992; 16: 621–4.Google Scholar
  4. 4.
    Peto R, Lopez AD, Boreham J, Thun M, Heath Jr. C, Mortality from Smoking in Developed Countries 1950–2000, Oxford: Oxford University Press, 1994.Google Scholar
  5. 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.Google Scholar
  6. 6.
    Davis DL, Dinse GE, Hoel DG. Decreasing cardiovascular disease and increasing cancer among whites in the United States from 1973 through 1987, JAMA, 1994; 271: 431–7.Google Scholar
  7. 7.
    Helbock HJ, Beckman KB, Shigenaga MK, Walter PB, Woodall AA, Yeo HC, Ames BN. DNA oxidation matters: The HPLC-electrochemical detection assay of 8-oxo-deoxyguanosine and 8-oxo-guanine. Proc Natl Acad Sci USA, 1998; 95: 288–293.Google Scholar
  8. 8.
    Von Sonntag C. The Chemical Basis of Radiation Biology, London: Taylor & Francis, 1987.Google Scholar
  9. 9.
    Stadtman ER Protein oxidation and aging, Science, 1992; 257: 1220–4.Google Scholar
  10. 10.
    Hankinson SE. Willett WC, Colditz GA, Seddon JM, Rosner B, Speizer FE, Stampfer MJ, A prospective study of cigarette smoking and risk of cataract surgery in women, JAMA, 1992; 268: 994–8.Google Scholar
  11. 11.
    Hankinson SE. Stampfer MJ, Seddon JM, Colditz GA, Rosner B, Speizer FE, Willett WC, Nutrient intake and cataract extraction in women: A prospective study, Br Med J, 1992; 305: 335–9.Google Scholar
  12. 12.
    Jacques PF, Hartz SC, Chylack LTJ, McGandy RB, Sadowski JA. Nutritional status in persons with and without senile cataract: Blood vitamin and mineral levels, Am J Clin Nutr, 1988; 48: 152–8.Google Scholar
  13. 13.
    Roe FJC, Lee PN, Conybeare G, Tobin G, Kelly D, Prentice D and Matter B, Risks of premature death and cancer predicted by body weight in early adult life, Hum Exp Toxicol, 1991; 10: 285–8.Google Scholar
  14. 14.
    Roe FJC, Non-genotoxic carcinogenesis: Implications for testing extrapolation to man, Mutagenesis, 1989; 4: 407–11.Google Scholar
  15. 15.
    Boutwell RK, Pariza MW, Historical perspectives: Calories and energy expenditure in carcinogenesis, Am J Clin Nutr, 1987; 45 (suppl): 151–6.Google Scholar
  16. 16.
    Youngman LD, Park J-YK, Ames BN, Protein oxidation associated with aging is reduced by dietary restriction of protein or calories, Proc Natl Acad Sci USA, 1992; 89: 9112–6.Google Scholar
  17. 17.
    Hunter DJ, Willett WC, Diet, body size, and breast cancer, Epidemiol Rev, 1993; 15: 110–32.Google Scholar
  18. 18.
    Swanson CA, Jones DY, Schatzkin A, Brinton LA, Ziegler RG, Breast cancer risk assessed by anthropometry in the NHANES I epidemiological follow-up study, Cancer Res, 1988; 48: 5363–7.Google Scholar
  19. 19.
    Willett WC, Stampfer MJ, Dietary fat and cancer: Another view, Cancer Causes Control, 1990; 1: 103.Google Scholar
  20. 20.
    Block G, Patterson B, Subar A, Fruit, vegetables and cancer prevention: A review of the epidemiologic evidence, Nutr Cancer 1992; 18: 1–29.Google Scholar
  21. 21.
    Steinmetz KA, Potter JD, Vegetables, fruit, and cancer. I. Epidemiology, Cancer Causes Control, 1991; 2: 325–57.Google Scholar
  22. 22.
    Hill MJ, Giacosa A, Caygill CPJ, ed., Epidemiology of Diet and Cancer, West Sussex: Ellis Horwood, 1994.Google Scholar
  23. 23.
    Howe GR, Hirohata T, Hislop TG, Dietary factors and risk of breast cancer: Combined analysis of 12 case-control studies, J Natl Cancer Inst, 1990; 82: 561–9.Google Scholar
  24. 24.
    Krebs-Smith SM, Cook A, Subar AF, Cleveland L, Friday J, Kahle LL. Fruit and vegetable intakes of children and adolescents in the United States. Arch Pediatr Adolesc Med, 1996; 150: 81–86.Google Scholar
  25. 25.
    Krebs-Smith SM, Cook A, Subar AF, Cleveland L, Friday J. US adults' fruit and vegetable intakes, 1989 to 1991: A revised baseline for the healthy people 2000 objective. Am J Public Health 1995; 85: 1623–1629.Google Scholar
  26. 26.
    Steinmetz KA, Potter JD, Vegetables, fruit, and cancer. II. Mechanisms, Cancer Causes Control, 1991; 2: 427–42.Google Scholar
  27. 27.
    MacGregor JT, Schlegel R, Wehr CM, Alperin P, Ames BN, Cytogenetic damage induced by folate deficiency in mice is enhanced by caffeine, Proc Natl Acad Sci USA, 1990; 87: 9962–5.Google Scholar
  28. 28.
    Blount BC, Mack MM, Wehr C, MacGregor J, Hiatt R, Wang G, Wickramasinghe SN, Everson RB, Ames BN. Folate deficiency causes uracil misincorporation into human DNA and chromosome breakage: Implications for cancer and neuronal damage. Proc Natl Acad Sci USA 1997; 94: 3290–3295.Google Scholar
  29. 29.
    Senti FR, Pilch SM, Analysis of folate data from the second National Health and Nutrition Examination Suvey (NHANES II), J Nutr, 1985; 115: 1398–402.Google Scholar
  30. 30.
    Bailey LB, Wagner PA, Christakis GJ, Araujo PE, Appledorf H, Davis CG, Masteryanni J, Dinning JS, Folacin and iron status and hematological findings in predominately black elderly persons from urban low-income households, Am J Clin Nutr, 1979; 32: 2346–53.Google Scholar
  31. 31.
    Bailey LB, Wagner PA, Christakis GJ, Davis CG, Appledorf H, Araujo PE, Dorsey E, Dinning JS, Folacin and iron status and hematological findings in black and Spanish-American adolescents from urban low-income households, Am J Clin Nutr, 1982; 35: 1023–32.Google Scholar
  32. 32.
    Bendich A, Butterworth Jr. CE, ed., Micronutrients in Health and in Disease Prevention New York, NY: Marcel Dekker, Inc., 1991.Google Scholar
  33. 33.
    Glynn SA, Albanes D, Folate and cancer: A review of the literature, Nutr Cancer 1994; 22: 101–19.Google Scholar
  34. 34.
    Giovannucci E, Stampfer MJ, Colditz GA, Rimm EB, Trichopoulos D, Rosner BA, Speizer FE, Willett WC, Folate, methionine, and alcohol intake and risk of colorectal adenoma, J Natl Cancer Inst, 1993; 85: 875–84.Google Scholar
  35. 35.
    Freudenheim JL, Graham S, Marshall JR, Haughey BP, Cholewinski S, Wilkinson G, Folate intake and carcinogenesis of the colon and rectum, Int J Epidemiol, 1991; 20: 368–74.Google Scholar
  36. 36.
    Wallock L, Woodall A, Jacob R, Ames B. Nutritional status and positive relation of plasma folate to fertility indices in nonsmoking men. FASEB Annual Meeting, Experimental Biology 97, New Orleans, LA, The FASEB J, 1997.Google Scholar
  37. 37.
    Rush D, Periconceptional folate and neural tube defect, Am J Clin Nutr, 1994; 59: 511S–6S.Google Scholar
  38. 38.
    Boushey CJ, Beresford SA, Omenn GS, Motulsky AG. A quantitative assessment of plasma homocysteine as a risk factor for vascular disease. Probable benefits of increasing folic acid intakes. J Am Med Assoc 1995; 274: 1049–57.Google Scholar
  39. 39.
    Safe SH, Dietary and environmental estrogens and antiestrogens and their possible role in human disease, Environ Sci Pollution Res, 1994; 1: 29–33.Google Scholar
  40. 40.
    Armstrong B, Doll R, Environmental factors and cancer incidence and mortality in different countries, with special reference to dietary practices, Int J Cancer, 1975; 15: 617–31.Google Scholar
  41. 41.
    Willett WC, Stampfer MJ, Colditz GA, Rosner BA, Speizer FE, Relation of meat, fat, and fiber intake to the risk of colon cancer in a prospective study among women, N Engl J Med, 1990; 323: 1664–72.Google Scholar
  42. 42.
    Giovannucci E, Rimm EB, Stampfer MJ, Colditz GA, Ascherio A, Willett WC, Intake of fat, meat, and fiber in relation to risk of colon cancer in men, Cancer Res, 1994; 54: 2390–7.Google Scholar
  43. 43.
    Goldbohm RA, van der Brandt PA, van't Veer P, Brants HAM, Dorant E, Sturmans F, Hermus RJJ, A prospective cohort study on the relation between meat consumption and the risk of colon cancer, Cancer Res 1994; 54: 718–23.Google Scholar
  44. 44.
    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.Google Scholar
  45. 45.
    Henderson BE, Ross RK, Pike MC, Toward the primary prevention of cancer, Science, 1991; 254: 1131–8.Google Scholar
  46. 46.
    Gerhardsson M, Floderus B, Norell SE, Physical activity and colon cancer risk, Int J Epidemiol, 1988; 17: 743–6.Google Scholar
  47. 47.
    Slattery ML, Schumacher MC, Smith KR, West DW, Abd-Eghany N, Physical activity, diet, and risk of colon cancer in Utah, Am J Epidemiol 1988; 128: 989–99.Google Scholar
  48. 48.
    Thun MJ, Calle EE, Namboodiri MM, Flanders WD, Coates RJ, Byers T, Boffetta P, Garfinkel L, Heath CWJ, Risk factors for fatal colon cancer in a large prospective study, J Natl Cancer Inst, 1992; 84: 1491–500.Google Scholar
  49. 49.
    International Agency for Research on Cancer, Alcohol Drinking, IARC Monograph Lyon, France: International Agency for Research on Cancer, 1988.Google Scholar
  50. 50.
    Giovannucci E, Rimm EB, Ascherio A, Stampfer MJ, Colditz GA, Willett WC, Alcohol, methyl-deficient diets and risk of colon cancer in men, J Natl Cancer Inst, 1995; 87: 265–73.Google Scholar
  51. 51.
    Sugimura T, Sato S, Ohgaki H, Takayama S, Nagao M, Wakabayashi K. Mutagens and carcinogens in cooked food. Prog Clin Biol Res, 1986; 206: 85–107.Google Scholar
  52. 52.
    International Agency for Research on Cancer, Some naturally occurring substances: Food Items and Constituents, Heterocyclic Aromatic Amines and Mycotoxins,IARC Monographs, Lyon, France: International Agency for Research on Cancer, 1993.Google Scholar
  53. 53.
    Peto R, Lopez AD, Boreham J, Thun M, Heath Jr. C, Mortality from tobacco in developed countries: Indirect estimation from national vital statistics, Lancet, 1992; 339: 1268–78.Google Scholar
  54. 54.
    Giovannucci E, Rimm EB, Stampfer MJ, Colditz GA, Ascherio A, Kearney J, Willett WC, A prospective study of cigarette smoking and risk of colorectal adenoma and colorectal cancer in U.S. men, J Natl Cancer Inst, 1994; 86: 183–91.Google Scholar
  55. 55.
    Giovannucci E, Colditz GA, Stampfer MJ, Hunter D, Rosner BA, Willett WC, Speizer FE, A prospective study of cigarette smoking and risk of colorectal adenoma and colorectal cancer in U.S. women, J Natl Cancer Inst, 1994; 86: 192–9.Google Scholar
  56. 56.
    Fielding JE, Preventing colon cancer: Yet another reason not to smoke, J Natl Cancer Inst, 1994; 86: 162–4.Google Scholar
  57. 57.
    US Environmental Protection Agency, Respiratory Health Effects of Passive Smoking: Lung Cancer and Other Disorders, Washington, DC: Office of Health and Environmental Assessment, Office of Research and Development, 1992.Google Scholar
  58. 58.
    Fontham ETH, Correa P, Reynolds P, Wu-Williams A, Buffler PA, Greenberg RS, Chen VW, Alterman T, Boyd P, Austin DF, Liff J, Environmental tobacco smoke and lung cancer in nonsmoking women, JAMA, 1994; 271: 1752–9.Google Scholar
  59. 59.
    Huber G, Brockie R, Mahajan V, Smoke and mirrors: The EPA's flawed study of environmental tobacco smoke and lung cancer, Regulation, 1993; 3: 46.Google Scholar
  60. 60.
    Schectman G, Byrd JC, Hoffmann R, Ascorbic acid requirements for smokers: Analysis of a population survey, Am J Clin Nutr, 1991; 53: 1466–70.Google Scholar
  61. 61.
    Duthie GG, Arthur JR, James WPT, Effects of smoking and vitamin E on blood antioxidant status, Am J Clin Nutr, 1991; 53: 1061S–3S.Google Scholar
  62. 62.
    Bui MH, Sauty A, Collet F, Leuenberger P, Dietary vitamin C intake and concentrations in the body fluids and cells of male smokers and nonsmokers, J Nutr, 1991; 122: 312–6.Google Scholar
  63. 63.
    Fraga CG, Motchnik PA, Shigenaga MK, Helbock HJ, Jacob RA, Ames BN, Ascorbic acid protects against endogenous oxidative damage in human sperm, Proc Natl Acad Sci USA, 1991; 88: 11003–6.Google Scholar
  64. 64.
    Woodall AA, Ames BN. Nutritional prevention of DNA damage to sperm and consequent risk reduction in birth defects and cancer in offspring. In: Bendich A and Deckelbaum R, eds., Preventative Nutrition: The Comprehensive Guide for Health Professionals, Totowa, NJ: Humana Press, 1997, pp. 373–385.Google Scholar
  65. 65.
    Ji B-T, Shu X-O, Linet MS, Zheng W, Wacholder S, Gao Y-T, Ying D-M, Jin F. Paternal cigarette smoking and the risk of childhood cancer among offspring of nonsmoking mothers. J Natl Cancer Inst 1997; 89: 238–244.Google Scholar
  66. 66.
    Shacter E, Beecham EJ, Covey JM, Kohn KW, Potter M, Activated neutrophils induce prolonged DNA damage in neighboring cells [published erratum appears in Carcinogenesis 1989 Mar; 10: 628], Carcinogenesis, 1998; 9: 2297–304.Google Scholar
  67. 67.
    Yamashina K, Miller BE, Heppner GH, Macrophage-mediated induction of drug-resistant variants in a mouse mammary tumor cell line, Cancer Res, 1986; 46: 2396–401.Google Scholar
  68. 68.
    Beasley RP, Hepatitis B virus, Cancer, 1987; 61: 1942–56.Google Scholar
  69. 69.
    Tabor E, Kobayashi K, Hepatitis C virus, a causative infectious agent of non-A, non-B hepatitis: Prevalence and structure. Summary of a conference on hepatitis C virus as a cause of hepatocellular carcinoma, J Natl Cancer Inst, 1992; 84: 86–90.Google Scholar
  70. 70.
    Yu M-W, You S-L, Chang A-S, Lu S-N, Liaw Y-F, Chen C-J, Association between hepatitis C virus antibodies and hepatocellular carcinoma in Taiwan, Cancer Res, 1991; 51: 5621–5.Google Scholar
  71. 71.
    Parkin DM, Suernsward J, Muir CS, Estimates of the world-wide frequency of twelve major cancers, Bull WHO, 1984; 62: 163–82.Google Scholar
  72. 72.
    Qian G-S, Ross RK, Yu MC, Yuan J-M, Gao Y-T, Henderson BE, Wogan GN, Groopman JD, A follow-up study of urinary markers of aflatoxin exposure and liver cancer risk in Shanghai, People's Republic of China, Cancer Epidemiol Biomarkers Prev, 1994; 3: 3–10.Google Scholar
  73. 73.
    Groopman JD, Zhu J, Donahue PR, Pikul A, Zhang L-S, Chen JS, Wogan GN, Molecular dosimetry of urinary afla-toxin DNA adducts in people living in Guangxi Autonomous Region, People's Republic of China, Cancer Res, 1992; 52: 45–51.Google Scholar
  74. 74.
    Pons WA, High pressure liquid chromatography determinations of aflatoxins in corn, J Assoc Off Anal Chem, 1979; 62: 584–6.Google Scholar
  75. 75.
    Yu MC, Tong MJ, Govindarajan S, Henderson BE, Nonviral risk factors for hepatocellular carcinoma in a low-risk population, the non-Asians of Los Angeles County, California, J Natl Cancer Inst, 1991; 83: 1820–6.Google Scholar
  76. 76.
    Yeh F-S, Yu MC, Mo C-C, Luo S, Tong MJ, Henderson BE, Hepatitis B virus, aflatoxins, and hepatocellular carcinoma in southern Guangxi, China, Cancer Res, 1989; 49: 2506–9.Google Scholar
  77. 77.
    International Agency for Research on Cancer, Schistosomes, Liver Flukes and Helicobacter pylori, IARC Monograph, Lyon, France: International Agency for Research on Cancer, 1994.Google Scholar
  78. 78.
    Howson C, Hiyama T, Wynder E, The decline in gastric cancer: Epidemiology of an unplanned triumph, Epidemiol Rev, 1986; 8: 1–27.Google Scholar
  79. 79.
    Korkina LG, Durnev AD, Suslova TB, Cheremisina ZP, Daugel-Dauge NO, Afanas'ev IB, Oxygen radical-mediated mutagenic effect of asbestos on human lymphocytes: Suppression by oxygen radical scavengers, Mutat Res, 1992; 265: 245–53.Google Scholar
  80. 80.
    Marsh JP, Mossman BT, Role of asbestos and active oxygen species in activation and expression of ornithine decarboxy-lase in hamster tracheal epithelial cells, Cancer Res, 1991; 51: 167–73.Google Scholar
  81. 81.
    Lowy DR, Kirnbauer R, Schiller JT, Genital human papil-lomavirus infection, Proc Natl Acad Sci USA, 1994; 91: 2436–40.Google Scholar
  82. 82.
    Jick H, Walker AM, Watkins RN, D'Ewart DC, Hunter JR, Danford A, Madsen S, Dinan BJ, Rothman KJ, Replacement estrogens and breast cancer, Am J Epidemiol, 1980; 112: 586–94.Google Scholar
  83. 83.
    Hankinson SE, Colditz GA, Hunter DJ, Spencer TL, Rosner B, Stampfer MJ, A quantitative assessment of oral contraceptive use and risk of ovarian cancer, Obstet Gynecol, 1992; 80: 708–14.Google Scholar
  84. 84.
    Harris JR, Lippman ME, Veronesi U, Willett W, Breast cancer, N Engl J Med, 1992; 327: 319–28.Google Scholar
  85. 85.
    Colditz GA, Stampfer MJ, Willett WC, Hunter DJ, Manson JE, Hennekens CH, Rosner BA, Speizer FE, Type of post-menopausal hormone use and risk of breast cancer: 12-year follow-up from the Nurses' Health Study, Cancer Causes Control, 1992; 3: 433–9.Google Scholar
  86. 86.
    Rosner B, Colditz G, Willett W, Reproductive risk factors in a prospective study of breast cancer: The Nurses' Health Study, Am J Epidemiol, 1994; 139: 819–35.Google Scholar
  87. 87.
    Russo J, Calaf G, Sohi N, Tahin Q, Zhang PL, Alvarado ME, Estrada S, Russo IH, Critical steps in breast carcinogenesis, Ann N Y Acad Sci, 1993; 698: 1–20.Google Scholar
  88. 88.
    Newcomb PA, Storer BE, Longnecker MP, Mittendorf R, Greenberg ER, Clapp RW, Burke KP, Willett WC, MacMahon B, Lactation and a reduced risk of premenopausal breast cancer, N Engl J Med, 1994; 330: 81–7.Google Scholar
  89. 89.
    Byers T, Graham S, Rzepka T, Marshall J, Lactation and breast cancer. Evidence for a negative association in pre-menopausal women, Am J Epidemiol, 1985; 121: 664–74.Google Scholar
  90. 90.
    Henderson B, Ross R, Pike M, Hormonal chemoprevention of cancer in women, Science, 1993; 259: 633–8.Google Scholar
  91. 91.
    Bernstein L, Henderson BE, Hanisch R, Sullivan-Halley J, Ross RK, Physical exercise and reduced risk of breast cancer in young women, J Natl Cancer Inst, 1994; 86: 1403–8.Google Scholar
  92. 92.
    Longnecker MP, Alcoholic beverage consumption in relation to risk of breast cancer: Meta-analysis and review, Cancer Causes Control, 1994; 5: 73–82.Google Scholar
  93. 93.
    Dorgan JF, Reichman ME, Judd JT, Brown C, Longcope C, Schatzkin A, Campbell WS, Franz C, Kahle L, Taylor PR, The relation of reported alcohol ingestion to plasma levels of estrogens and androgens in premenopausal women (Maryland, United States), Cancer Causes Control, 1994; 5: 53–60.Google Scholar
  94. 94.
    International Agency for Research on Cancer, Some Industrial Chemicals, IARC Monographs, Lyon, France: International Agency for Research on Cancer, 1994.Google Scholar
  95. 95.
    Connelly RR, Spirtas R, Myers MH, Percy CL, Fraumeni Jr JF, Demographic patterns for mesothelioma in the United States, J Natl Cancer Inst, 1987; 78: 1053–60.Google Scholar
  96. 96.
    Reynolds T, Asbestos-linked cancer rates up less than predicted., J Nat Cancer Inst, 1992; 84: 560–2.Google Scholar
  97. 97.
    Ames BN, Gold LS, Chemical carcinogenesis: Too many rodent carcinogens, Proc Natl Acad Sci USA, 1990; 87: 7772–6.Google Scholar
  98. 98.
    Ames BN, Shigenaga MK, Gold LS, DNA lesions, inducible DNA repair, and cell division: Three key factors in mutagenesis and carcinogenesis, Environ Health Perspect, 1993; 35–44.Google Scholar
  99. 99.
    Gold LS, Garfinkel GB, Slone TH, Setting priorities among possible carcinogenic hazards in the workplace, in: Smith CM, Christiani DC, Kelsey KT, eds., Chemical Risk Assessment and Occupational Health, Current Applications, Limitations, and Future Prospects, Westport, CT: Greenwood Publishing Group, 1994.Google Scholar
  100. 100.
    International Agency for Research on Cancer, Solar and Ultraviolet Radiation, IARC Monograph, Lyon, France: International Agency for Research on Cancer, 1992.Google Scholar
  101. 101.
    Ellis M, Lisher M, Second malignancies following treatment in non-Hodgkin's lymphoma, Leuk Lymphoma, 1993; 9: 337–42.Google Scholar
  102. 102.
    International Agency for Research on Cancer, Overall Evaluations of Carcinogenicity: An Updating of IARC Mono-graphs Volumes 1 to 42. Suppl. 7, IARC Monographs, Lyon, France: International Agency for Research on Cancer, 1987.Google Scholar
  103. 103.
    Ryffel B, The carcinogenicity of cyclosporin, Toxicology, 1992; 73: 1–22.Google Scholar
  104. 104.
    Preston-Martin S, Thomas DC, Yu MC, Henderson BE, Diagnostic radiography as a risk factor for chronic myeloid and monocytic leukaemia (CML), Br J Cancer, 1989; 59: 639–44.Google Scholar
  105. 105.
    Gough M, How much cancer can EPA regulate anyway?, Risk Anal, 1990; 10: 1–6.Google Scholar
  106. 106.
    Pershagen G, Akerblom G, Axelson O, Clavensjo B, Damber L, Desai G, Enflo A, Lagarde F, Mellander H, Swartengren M, Swedjemark GA, Residential radon exposure and lung cancer in Sweden, N Engl J Med, 1994; 330: 159–64.Google Scholar
  107. 107.
    Nero AV, A national strategy for indoor radon, Issues in Sci and Tech, 1992; 9: 33–40.Google Scholar
  108. 108.
    Lubin JH, Boice Jr. JD, Elding C, Hornint RW, Howe G, Kunz E, Kusiak RA, Morrison HI, Radford EP, Samet JM, Tirmarche M, Woodward A, Xiang YS, Pierce DA, Radon and lung cancer risk: a joint analysis of 11 underground miner studies, U.S. Department of Health and Human Services, NIH Publication No. 94–3644, 1994.Google Scholar
  109. 109.
    Lètourneau EG, Krewski D, Choi NW, Goddard MJ, McGregor RG, Zielinski JM, Du J, Case-control study of residential radon and lung cancer in Winnipeg, Manitoba, Canada, Am J Epidemiol, 1994; 140: 310–22.Google Scholar
  110. 110.
    Lubin JH, Invited commentary: Lung cancer and exposure to residential radon, Am J Epidemiol, 1994; 140: 323–32.Google Scholar
  111. 111.
    Nero A, Developing a methodology for identifying high-radon areas, Center for Building Science News (Lawrence Berkeley Laboratory), 1994; 1: 4–5.Google Scholar
  112. 112.
    Smith AH, Hopenhayn RC, Bates MN, Goeden HM, Hertz PI, Duggan HM, Wood R, Kosnett MJ, Smith MT, Cancer risks from arsenic in drinking water, Environ Health Perspect, 1992; 97: 259–67.Google Scholar
  113. 113.
    Bates MN, Smith AH, Hopenhayn RC, Arsenic ingestion and internal cancers: A review, Am J Epidemiol 1992; 135: 462–76.Google Scholar
  114. 114.
    International Agency for Research on Cancer, Chlorinated drinking-water; chlorination by-products; some other halo-genated compounds; cobalt and cobalt compounds, IARC Monograph, Lyon, France: International Agency for Research on Cancer, 1991.Google Scholar
  115. 115.
    Knudsen A, Hereditary cancers: Clues to mechanisms of carcinogenesis, Brit J Cancer, 1989; 59: 661–6.Google Scholar
  116. 116.
    Ponder B, Inherited predisposition to cancer, Trends in Genetics, 1990; 6: 213–8.Google Scholar
  117. 117.
    Gold Ls, Slone TH, Stern BR, Manley NB, Ames BN, Rodent carcinogens: Setting priorities, Science, 1992 258: 261–5.Google Scholar
  118. 118.
    Carson R, Silent Spring, Boston, MA: Houghton-Mifflin, 1962.Google Scholar
  119. 119.
    Gold LS, Slone TH, Ames BN. Overview and update analyses of the carcinogenic potency database, in: Gold LS and Zeiger E, eds., Handbook of Carcinogenic Potency and Genotoxicity Databases, Boca Raton, FL: CRC Press, 1997; pp. 661–685.Google Scholar
  120. 120.
    Gold LS, Stern BR, Slone TH, Brown JP, Manley NB, Ames BN, Pesticide residues in food: Investigation of disparities in cancer risk estimates, Cancer Lett, 1997; 117: 195–207.Google Scholar
  121. 121.
    Ames BN, Profet M, Gold LS, Dietary pesticides (99.99% all natural), Proc Natl Acad Sci USA 1990; 87: 7777–81.Google Scholar
  122. 122.
    Patterson BH, Block G, Food choices and the cancer guidelines, Am J Public Health 1988; 78: 282–6.Google Scholar
  123. 123.
    Key T, Reeves G, Organochlorines in the environment and breast cancer, Br Med J, 1994; 308: 1520–1.Google Scholar
  124. 124.
    Ames BN, Profet M, Gold LS, Nature's chemicals and synthetic chemicals: Comparative toxicology, Proc Natl Acad Sci USA, 1990; 87: 7782–6.Google Scholar
  125. 125.
    Crandall R, Why is the cost of environmental regulation so high?, Center for the Study of American Business, 110, 1992.Google Scholar
  126. 126.
    Bartlett B, The High Cost of Turning Green, The Wall Street Journal, Sept. 14, 1994.Google Scholar
  127. 127.
    Ames BN, Gold LS, Environmental pollution, pesticides, and the prevention of cancer: Misconceptions, FASEB J, 1997; 11: 1041–1052.Google Scholar
  128. 128.
    Tengs TO, Adams ME, Pliskin JS, Safran DG, Siegel JE, Weinstein MC, Graham JD, Five-hundred life-saving interventions and their cost-effectiveness, Risk Anal, 1995; 15: 369–89.Google Scholar
  129. 129.
    Keeney RL, Mortality risks induced by economic expenditures, Risk Anal., 1990; 10: 147–59.Google Scholar
  130. 130.
    Wildavsky A, Searching for Safety, New Brunswick, N.J.: Transaction Press, 1988.Google Scholar
  131. 131.
    Viscusi WK, Fatal Trade-offs, Oxford, England: Oxford University Press, 1992.Google Scholar
  132. 132.
    Breyer S, Breaking the Vicious Cycle: Toward Effective Risk Regulation, Cambridge, MA: Harvard University Press, 1993.Google Scholar
  133. 133.
    Willett WC, Diet, nutrition and avoidable cancer, Environ Health Perspect, 1995; 103 (Suppl 8): 165–70.Google Scholar
  134. 134.
    Phillips RL, Garfinkel L, Kuzma JW, Beeson WL, Lotz T, Brin B, Mortality among California Seventh-day Adventists for selected cancer sites, J Natl Cancer Inst, 1980; 65: 1097–107.Google Scholar
  135. 135.
    Mills PK, Beeson WL, Phillips RL, Fraser GE, Cancer incidence among California Seventh-day Adventists, Am J Clin Nutr, 1994; 59: 1136S–42S.Google Scholar
  136. 136.
    Ames BN, Gold LS, Willett WC, The causes and prevention of cancer, Proc Natl Acad Sci USA, 1995; 92: 5258–65.Google Scholar
  137. 137.
    Ames BN, Gold LS, The causes and prevention of cancer: The role of environment, in: Bailey R, ed., The True State of the Planet, New York, NY: Free Press, 1995, pp.141–175.Google Scholar

Copyright information

© Kluwer Academic Publishers 1998

Authors and Affiliations

  • Bruce N. Ames
    • 1
  • Lois Swirsky Gold
    • 2
  1. 1.Department of Molecular and Cell BiologyUniversity of CaliforniaBerkeley
  2. 2.Life Sciences DivisionE.O. Lawrence Berkeley National LaboratoryBerkeley

Personalised recommendations