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.

  • Progress
  • Published:

Cancer epidemiology in the last century and the next decade

Abstract

By the early 1980s, epidemiologists had identified many important causes of cancer. They had also proposed the 'multi-stage' model of cancer, although none of the hypothesized events in human carcinogenesis had then been identified. The remarkable advances in cell and molecular biology over the past two decades have transformed the scope and methods of cancer epidemiology. There have been a few new discoveries based purely on traditional methods, and many long-suspected minor risks have been estimated more precisely. But modern epidemiological studies often depend on genetic, biochemical or viral assays that had not been developed 20 years ago.

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: Cancer rates in migrants become similar to those in the local population.
Figure 2: Smoking kills different populations in different ways.
Figure 3: Age has no effect on susceptibility to some carcinogens.
Figure 4: Global cancer incidence in developed and developing countries.

Similar content being viewed by others

References

  1. Doll, R. & Peto, R. The causes of cancer: quantitative estimates of avoidable risks of cancer in the United States today. J. Natl Cancer Inst. 66, 1191–1308 (1981).

    Article  CAS  PubMed  Google Scholar 

  2. World Health Organization. Prevention of Cancer (WHO Tech. Rep. 276) (WHO, Geneva, 1964).

  3. Doll, R. An epidemiological perspective of the biology of cancer. Cancer Res. 38, 3573–3583 (1978).

    CAS  PubMed  Google Scholar 

  4. Peto, R., Lopez, A. D., Boreham, J., Heath, C. & Thun, M. Mortality from Tobacco in Developed Countries, 1950–2000 (Oxford Univ. Press, Oxford, 1994).

    Google Scholar 

  5. Doll, R. & Hill, A. B. Smoking and carcinoma of the lung. Preliminary report. Br. Med. J. ii, 739–748 (1950).

    Article  Google Scholar 

  6. Wynder, E. L. & Graham, E. A. Tobacco smoking as a possible etiologic factor in bronchogenic carcinoma. J. Am. Med. Assoc. 143, 329–336 (1950).

    Article  CAS  PubMed  Google Scholar 

  7. Wald, N., Doll, R. & Copeland, G. Trends in tar, nicotine, and carbon monoxide yields of UK cigarettes manufactured since 1934. Br. Med. J. (Clin. Res. Ed.) 282, 763–765 (1981).

    Article  CAS  Google Scholar 

  8. Peto, R. et al. Smoking, smoking cessation, and lung cancer in the UK since 1950: combination of national statistics with two case-control studies. Br. Med. J. 321, 323–329 (2000).

    Article  CAS  Google Scholar 

  9. Doll, R. Cancers weakly related to smoking. Br. Med. Bull. 52, 35–49 (1996).

    Article  CAS  PubMed  Google Scholar 

  10. Doll, R. & Peto, R. in Oxford Textbook of Medicine 4th edn (eds Warrell, D. A., Cox, T. M. & Firth, J. D.) (Oxford Medical Publications, Oxford, in the press).

  11. Liu, B. Q. et al. Emerging tobacco hazards in China: 1. Retrospective proportional mortality study of one million deaths. Br. Med. J. 317, 1411–1422 (1998).

    Article  CAS  Google Scholar 

  12. Peto, R., Lopez, A. D., Boreham, J., Thun, M. & Heath, C. Mortality from tobacco in developed countries: indirect estimation from national vital statistics. Lancet 339, 1268–1278 (1992).

    Article  CAS  PubMed  Google Scholar 

  13. Working Group on Diet and Cancer of the Committee on Medical Aspects of Food and Nutrition Policy. Nutritional Aspects of the Development of Cancer (Dept Health Rep. Health Social Subjects 48) (The Stationery Office, London, 1998).

  14. IARC. Some Naturally Occurring Substances: Food Items and Constituents, Heterocyclic Aromatic Amines and Mycotoxins (IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, 56) (IARC, Lyon, 1993).

  15. American Institute for Cancer Research/World Cancer Research Fund. Food, Nutrition and the Prevention of Cancer: A Global Perspective (American Institute for Cancer Research, Washington, 1997).

  16. Josefson, D. Obesity and inactivity fuel global cancer epidemic. Br. Med. J. 322, 945 (2001).

  17. Bergstrom, A., Pisani, P., Tenet, V., Wolk, A. & Adami, H. O. Overweight as an avoidable cause of cancer in Europe. Int. J. Cancer 91, 421–430 (2001).

    Article  CAS  PubMed  Google Scholar 

  18. Calle, E. E., Thun, M. J., Petrelli, J. M., Rodriguez, C. & Heath, C. W. Body-mass index and mortality in a prospective cohort of U.S. adults. N. Engl. J. Med. 341, 1097–1105 (1999).

    Article  CAS  PubMed  Google Scholar 

  19. Hennekens, C. H. et al. Lack of effect of long-term supplementation with beta carotene on the incidence of malignant neoplasms and cardiovascular disease. N. Engl. J. Med. 334, 1145–1149 (1996).

    Article  CAS  PubMed  Google Scholar 

  20. Alpha-Tocopherol, Beta Carotene Cancer Prevention Study Group. The effect of vitamin E and beta carotene on the incidence of lung cancer and other cancers in male smokers. N. Engl. J. Med. 330, 1029–1035 (1994).

  21. Omenn, G. S. et al. Effects of a combination of beta carotene and vitamin A on lung cancer and cardiovascular disease. N. Engl. J. Med. 334, 1150–1155 (1996).

    Article  CAS  PubMed  Google Scholar 

  22. Janne, P. A. & Mayer, R. J. Chemoprevention of colorectal cancer. N. Engl. J. Med. 342, 1960–1968 (2000).

    Article  CAS  PubMed  Google Scholar 

  23. Hankinson, S. E. et al. Plasma sex steroid hormone levels and risk of breast cancer in postmenopausal women. J. Natl Cancer Inst. 90, 1292–1299 (1998).

    Article  CAS  PubMed  Google Scholar 

  24. Hankinson, S. E. et al. Plasma prolactin levels and subsequent risk of breast cancer in postmenopausal women. J. Natl Cancer Inst. 91, 629–634 (1999).

    Article  CAS  PubMed  Google Scholar 

  25. IARC. Hormonal Contraception and Post-Menopausal Hormonal Therapy (IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, 72) (IARC, Lyon, 1999).

  26. Casagrande, J. T. et al. 'Incessant ovulation' and ovarian cancer. Lancet 2, 170–173 (1979).

    Article  CAS  PubMed  Google Scholar 

  27. Pike, M. C., Krailo, M. D., Henderson, B. E., Casagrande, J. T. & Hoel, D. G. 'Hormonal' risk factors, 'breast tissue age' and the age-incidence of breast cancer. Nature 303, 767–770 (1983).

    Article  ADS  CAS  PubMed  Google Scholar 

  28. Newcomb, P. A. et al. Lactation and a reduced risk of premenopausal breast cancer. N. Engl. J. Med. 330, 81–87 (1994).

    Article  CAS  PubMed  Google Scholar 

  29. Swerdlow, A. J. in Principles and Practice of Genitourinary Oncology (eds Raghavan, D., Scher, H. I., Leibel, S. A. & Lange, P.) 643–652 (Lippincott-Raven, New York, 1997).

    Google Scholar 

  30. IARC. Schistosomes, Liver Flukes and Heliobacter pylori (IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, 61) (IARC, Lyon, 1994).

  31. Walboomers, J. M. et al. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J. Pathol. 189, 12–19 (1999).

    Article  CAS  PubMed  Google Scholar 

  32. IARC. Human Papillomaviruses (IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, 64) (IARC, Lyon, 1995).

  33. IARC. Hepatitis Viruses (IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, 59) (IARC, Lyon, 1994).

  34. Parkin, D. M., Pisani, P., Munoz, N. & Ferlay, J. The global health burden of infection associated cancers. Cancer Surv. 33, 5–33 (1999).

    Google Scholar 

  35. IARC. Epstein-Barr Virus and Kaposi's Sarcoma Herpesvirus/Human Herpesvirus 8 (IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, 70) (IARC, Lyon, 1997).

  36. IARC. Human Immunodeficiency Viruses and Human T-cell Lymphotropic Viruses (IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, 67) (IARC, Lyon, 1996).

  37. Kinlen, L. J. Infection and childhood leukemia. Cancer Causes Cont. 9, 237–239 (1998).

    Article  CAS  Google Scholar 

  38. Carbone, M., Rizzo, P. & Pass, H. Simian virus 40: the link with human malignant mesothelioma is well established. Anticancer Res. 20, 875–877 (2000).

    CAS  PubMed  Google Scholar 

  39. Kinlen, L. J., Sheil, A. G., Peto, J. & Doll, R. Collaborative United Kingdom-Australasian study of cancer in patients treated with immunosuppressive drugs. Br. Med. J. 2, 1461–1466 (1979).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Birkeland, S. A. et al. Cancer risk after renal transplantation in the Nordic countries, 1964-1986. Int. J. Cancer 60, 183–189 (1995).

    Article  CAS  PubMed  Google Scholar 

  41. Peto, J., Decarli, A., La Vecchia, C., Levi, F. & Negri, E. The European mesothelioma epidemic. Br. J. Cancer 79, 666–672 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Wagner, J. C., Sleggs, C. A. & Marchand, P. Diffuse pleural mesothelioma and asbestos exposure in the North Western Cape Province. Br. J. Ind. Med. 17, 260–271 (1960).

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Doll, R. Mortality from lung cancer in asbestos workers. Br. J. Ind. Med. 12, 81–86 (1955).

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Venitt, S. & Phillips, D. H. in Environmental Mutagenesis (eds Phillips, D. H. & Venitt, S.) 1–20 (Bios Scientific, Oxford, 1995).

    Google Scholar 

  45. Dockery, D. W. et al. An association between air pollution and mortality in six U.S. cities. N. Engl. J. Med. 329, 1753–1759 (1993).

    Article  CAS  PubMed  Google Scholar 

  46. Hein, D. W. et al. Molecular genetics and epidemiology of the NAT1 and NAT2 acetylation polymorphisms. Cancer Epidemiol. Biomarkers Prev. 9, 29–42 (2000).

    CAS  PubMed  Google Scholar 

  47. Cartwright, R. A. et al. Role of N-acetyltransferase phenotypes in bladder carcinogenesis: a pharmacogenetic epidemiological approach to bladder cancer. Lancet 2, 842–845 (1982).

    Article  CAS  PubMed  Google Scholar 

  48. Doll, R. Possibilities for the Prevention of Cancer (Royal Society Lecture for the Public, 13 November 1986) (Royal Society, London).

  49. Johns, L. E. & Houlston, R. S. Glutathione S-transferase μ1 (GSTM1) status and bladder cancer risk: a meta-analysis. Mutagenesis 15, 399–404 (2000).

    Article  CAS  PubMed  Google Scholar 

  50. Houlston, R. S. Glutathione S-transferase M1 status and lung cancer risk: a meta-analysis. Cancer Epidemiol. Biomarkers Prev. 8, 675–682 (1999).

    CAS  PubMed  Google Scholar 

  51. Dunning, A. M. et al. A systematic review of genetic polymorphisms and breast cancer risk. Cancer Epidemiol. Biomarkers Prev. 8, 843–854 (1999).

    CAS  PubMed  Google Scholar 

  52. Woodage, T. et al. The APCI1307K allele and cancer risk in a community-based study of Ashkenazi Jews. Nature Genet. 20, 62–65 (1998).

    Article  CAS  PubMed  Google Scholar 

  53. Krontiris, T. G., Devlin,B., Karp, D. D., Robert, N. J. & Risch, N. An association between the risk of cancer and mutations in the HRAS1 minisatellite locus. N. Engl. J. Med. 329, 517–523 (1993).

    Article  CAS  PubMed  Google Scholar 

  54. Bennett, W. P. et al. Environmental tobacco smoke, genetic susceptibility, and risk of lung cancer in never-smoking women. J. Natl Cancer Inst. 91, 2009–2014 (1999).

    Article  CAS  PubMed  Google Scholar 

  55. Ambrosone, C. B. et al. Cigarette smoking, N-acetyltransferase 2 genetic polymorphisms, and breast cancer risk. J. Am. Med. Assoc. 276, 1494–1501 (1996).

    Article  CAS  Google Scholar 

  56. Weinberg, C. R. & Sandler, D. P. Gene-by-environment interaction for passive smoking and glutathione S-transferase M1? J. Natl Cancer Inst. 91, 1985–1986 (1999).

    Article  CAS  PubMed  Google Scholar 

  57. IARC. Tobacco Smoking (IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, 38) (IARC, Lyon, 1986).

  58. Ma, J. et al. Methylenetetrahydrofolate reductase polymorphism, dietary interactions, and risk of colorectal cancer. Cancer Res. 57, 1098–1102 (1997).

    CAS  PubMed  Google Scholar 

  59. Houlston, R. S. & Peto, J. in Genetic Predisposition to Cancer (eds Eeles, R. A., Ponder, B. A. J., Easton, D. F. & Horwich, A.) 208–226 (Chapman & Hall, London, 1996).

    Book  Google Scholar 

  60. Peto, J. in Cancer Incidence in Defined Populations. Banbury Report 4 (eds Cairns, J., Lyon, J. L. & Skolnick, M.) 203–213 (Cold Spring Harbor Laboratory Press, 1980).

    Google Scholar 

  61. Peto, J. & Mack, T. M. High constant incidence in twins and other relatives of women with breast cancer. Nature Genet. 26, 411–414 (2000).

    Article  CAS  PubMed  Google Scholar 

  62. Ford, D. et al. Genetic heterogeneity and penetrance analysis of the BRCA1 and BRCA2 genes in breast cancer families. The Breast Cancer Linkage Consortium. Am. J. Hum. Genet. 62, 676–689 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Peto, J. et al. Prevalence of BRCA1 and BRCA2 gene mutations in patients with early-onset breast cancer. J. Natl Cancer Inst. 91, 943–949 (1999).

    Article  CAS  PubMed  Google Scholar 

  64. Peto, R., Parish, S. E. & Gray, R. G. in Age-Related Factors in Carcinogenesis (IARC Sci. Publ. 58) (eds Likhachev, A., Anisimov, V. & Montesano, R.) 43–53 (IARC, Lyon, 1986).

    Google Scholar 

  65. Peto, J. in Models, Mechanisms and Aetiology of Tumour Promotion (IARC Sci. Publ. 56) (eds Borzsonyi, M., Day, N. E., Lapis, K. & Yamasaki, H.) 359–371 (IARC, Lyon, 1984).

    Google Scholar 

  66. DePinho, R. A. The age of cancer. Nature 408, 248–254 (2000).

    Article  ADS  CAS  PubMed  Google Scholar 

  67. Halpern, M. T., Gillespie, B. W. & Warner, K. E. Patterns of absolute risk of lung cancer mortality in former smokers. J. Natl Cancer Inst. 85, 457–464 (1993).

    Article  CAS  PubMed  Google Scholar 

  68. Janin, N. A simple model for carcinogenesis of colorectal cancers with microsatellite instability. Adv. Cancer Res. 77, 189–221 (2000).

    Article  CAS  PubMed  Google Scholar 

  69. Pankow, J. S. et al. Genetic analysis of mammographic breast density in adult women: evidence of a gene effect. J. Natl Cancer Inst. 89, 549–556 (1997).

    Article  CAS  PubMed  Google Scholar 

  70. Roberts, S. A. et al. Heritability of cellular radiosensitivity: a marker of low-penetrance predisposition genes in breast cancer? Am. J. Hum. Genet. 65, 784–794 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Berwick, M. & Vineis, P. Markers of DNA repair and susceptibility to cancer in humans: an epidemiologic review. J. Natl Cancer Inst. 92, 874–897 (2000).

    Article  CAS  PubMed  Google Scholar 

  72. Bonassi, S. et al. Chromosomal aberrations in lymphocytes predict human cancer independently of exposure to carcinogens. European Study Group on Cytogenetic Biomarkers and Health. Cancer Res. 60, 1619–1625 (2000).

    CAS  PubMed  Google Scholar 

  73. Anker, P., Mulcahy, H., Chen, X. Q. & Stroun, M. Detection of circulating tumour DNA in the blood (plasma/serum) of cancer patients. Cancer Metastasis Rev. 18, 65–73 (1999).

    Article  CAS  PubMed  Google Scholar 

  74. Ponten, F. et al. Molecular pathology in basal cell cancer with p53 as a genetic marker. Oncogene 15, 1059–1067 (1997).

    Article  CAS  PubMed  Google Scholar 

  75. Khrapko, K. et al. Constant denaturant capillary electrophoresis (CDCE): a high resolution approach to mutational analysis. Nucleic Acids Res. 22, 364–369 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. zur Hausen, H. Proliferation-inducing viruses in non-permissive systems as possible causes of human cancers. Lancet 357, 381–384 (2001).

    Article  PubMed  Google Scholar 

  77. Parkin, D. M., Bray, F. I. & Devesa, S. S. Cancer burden in the year 2000. The global picture. Eur.J.Cancer (special supplement; in the press).

  78. Schiller, J. T. & Lowy, D. R. Papillomavirus-Like Particle Vaccines. J. Natl Cancer Inst. Monogr. 28, 50–54 (2000).

    Article  Google Scholar 

  79. Cullen, M. R. Chrysotile asbestos: enough is enough. Lancet 351, 1377–1378 (1998).

    Article  CAS  PubMed  Google Scholar 

  80. McDonald, A. D. et al. Mesothelioma in Quebec chrysotile miners and millers: epidemiology and aetiology. Ann. Occup. Hyg. 41, 707–719 (1997).

    Article  CAS  PubMed  Google Scholar 

  81. Black, D. et al. HIV testing on all pregnant women. Lancet 2, 1277 (1987).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Parts of the section on environmental and lifestyle factors are based on the review on avoidable causes of cancer by Richard Doll and my brother Richard Peto1 and their updated summary10. I am also grateful to them and to many other colleagues for commenting on earlier drafts, and to the Cancer Research Campaign for support.

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Peto, J. Cancer epidemiology in the last century and the next decade. Nature 411, 390–395 (2001). https://doi.org/10.1038/35077256

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/35077256

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing