Cancer epidemiology in the last century and the next decade

Article metrics

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.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

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.

References

  1. 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).

  2. 2

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

  3. 3

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

  4. 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).

  5. 5

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

  6. 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).

  7. 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).

  8. 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).

  9. 9

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

  10. 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. 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).

  12. 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).

  13. 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. 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. 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. 16

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

  17. 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).

  18. 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).

  19. 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).

  20. 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. 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).

  22. 22

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

  23. 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).

  24. 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).

  25. 25

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

  26. 26

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

  27. 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).

  28. 28

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

  29. 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).

  30. 30

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

  31. 31

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

  32. 32

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

  33. 33

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

  34. 34

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

  35. 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. 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. 37

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

  38. 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).

  39. 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).

  40. 40

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

  41. 41

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

  42. 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).

  43. 43

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

  44. 44

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

  45. 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).

  46. 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).

  47. 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).

  48. 48

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

  49. 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).

  50. 50

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

  51. 51

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

  52. 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).

  53. 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).

  54. 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).

  55. 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).

  56. 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).

  57. 57

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

  58. 58

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

  59. 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).

  60. 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).

  61. 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).

  62. 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).

  63. 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).

  64. 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).

  65. 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).

  66. 66

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

  67. 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).

  68. 68

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

  69. 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).

  70. 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).

  71. 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).

  72. 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).

  73. 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).

  74. 74

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

  75. 75

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

  76. 76

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

  77. 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. 78

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

  79. 79

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

  80. 80

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

  81. 81

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

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

Rights and permissions

Reprints and Permissions

About this article

Further reading

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.