Nature 280, 361 - 367 (02 August 1979); doi:10.1038/280361a0

Population biology of infectious diseases: Part I

Roy M. Anderson^* & Robert M. May^†

^*Zoology Department and Centre for Environmental Technology, Imperial College, London University, London SW7, UK
^†Biology Department, Princeton University, Princeton, New Jersey 08544

If the host population is taken to be a dynamic variable (rather than constant, as conventionally assumed), a wider understanding of the population biology of infectious diseases emerges. In this first part of a two-part article, mathematical models are developed, shown to fit data from laboratory experiments, and used to explore the evolutionary relations among transmission parameters. In the second part of the article, to be published in next week's issue, the models are extended to include indirectly transmitted infections, and the general implications for infectious diseases are considered.

References

1.	Park, T. Ecol. Monogr. 18, 267–307 (1948).
2.	Lanciani, C. A. Ecology 56, 689–695 (1975).
3.	Davis, J. W. & Anderson, R. C. (eds) Parasitic Diseases of Wild Mammals (Iowa State University Press, 1971).
4.	Naumov, N. P. The Ecology of Animals, Ch. 17 (University of Illinois Press, Chicago, 1972).
5.	Davis, J. W., Anderson, R. C., Karstad, L. & Trainer, D. O. (eds) Infectious and Parasitic Diseases of Wild Birds (Iowa State University Press, 1971).
6.	Jennings, A. R. J. comp. Path. 64, 356–359 (1954).
7.	Jennings, A. R. Bird Study 8, 25–31 (1961).
8.	Forrester, D. J. in Parasitic Diseases of Wild Mammals (eds Davis, J. W. & Anderson, R. C.) 158–173 (Iowa State University Press, 1971).
9.	Uhazy, L. S., Holmes, J. C. & Stelfax, J. G. Can. J. Zool. 51, 817–824 (1973).
10.	Pearsall, W. H. New Biol. 17, 9–26 (1954).
11.	Hilborn, R. and Sinclair, A. R. E. in Serengeti: Dynamics of an Ecosystem (eds Sinclair, A. R. W. & Norton-Griffiths, M.) (University of Chicago Press, 1979).
12.	Price, P. W. Evolutionary Biology of Parasites (Princeton University Press, 1979).
13.	Anderson, R. M. in Population Dynamics (eds Anderson, R. M., Turner, B. D. & Taylor, L. R.) (Blackwell, Oxford, 1979).
14.	Crofton, H. D. Parasitology 63, 179–193 (1971).
15.	Crofton, H. D. Parasitology 63, 343–364 (1971).
16.	Anderson, R. M. & May, R. M. J. Anim. Ecol. 47, 219–247 (1978).
17.	May, R. M. & Anderson, R. M. J. Anim. Ecol. 47, 249–267 (1978).
18.	Barbehenn, K. R. Biotropica 1, 29–35 (1969).
19.	Cornell, H. Am. Nat. 108, 880–883 (1974).
20.	Carey, A. B. Ecol. Monogr. (in the press).
21.	Bradley, D. J. in Origins of Pest, Parasite, Disease and Weed Problems (eds Cherrett, J. M. & Sagar, G. R.) (Blackwell, Oxford, 1977).
22.	Latham, M. C. Science 188, 561–565 (1975).
23.	McNeill, W. H. Plagues and People (Blackwell, Oxford, 1976).
24.	Fenner, F. in The Impact of Civilization on the Biology of Man (ed. Boyden, S. W.) (University of Toronto Press, 1970).
25.	Black, F. L. Science 187, 515–518 (1975).
26.	Bailey, N. T. J. The Mathematical Theory of Infectious Diseases 2nd edn (Macmillan, New York, 1975).
27.	Macdonald, G. The Epidemiology and Control of Malaria (Oxford University Press, 1957).
28.	Macdonald, G. Dynamics of Tropical Disease (eds Bruce-Chwatt, L. J. & Glanville, V. J.) (Oxford University Press, 1973).
29.	Bartlett, M. S. Stochastic Population Models in Ecology and Epidemiology (Methuen, Londan ,1960).
30.	Dietz, K. J. R. Stat. Soc. A 130, 505–528 (1967).
31.	Waltman, P. Deterministic Threshold Models in the Theory of Epidemics (Lecture Notes in Biomathematics Vol. 1) (Springer, New York, 1974).
32.	Yorke, J. A., Nathanson, N., Pianigiani, G. & Martin, J. Am. J. Epidem. 108, 103–123 (1979).
33.	Hoppensteadt, F. C. Mathematical Theories of Populations: Demographics, Genetics, and Epidemics (SIAM, Philadelphia, 1976).
34.	Dietz, K. in Epidemiology (eds Ludwig, D. & Cooke, K. L.) 104–121 (Society for Industrial and Applied Mathematics, Philadelphia, 1975).
35.	Anderson, R. M. Parasitology 76, 119–157 (1978).
36.	May, R. M. & Anderson, R. M. Nature (next week's issue).
37.	Mimms, C. A. The Pathogenesis of Infectious Diseases (Academic, London, 1977).
38.	Kimberlin, R. H. (ed.) Slow Virus Diseases of Animals and Man (North-Holland, Amsterdam, 1976).
39.	Wabelin, D. J. Nature 273, 617–620 (1978).
40.	Soulsby, E. J. L. (ed.) Immunity to Animal Parasites (Academic, London, 1972).
41.	Fine, P. E. M. Ann. N.Y. Acad. Sci. 266, 173–194 (1975).
42.	Stiven, A. E. Ecol. Monogr. 34, 119–142 (1964).
43.	Hines, R. S. & Spira, D. T. J. Fish Biol. 5, 385–392 (1973).
44.	Robinson, G. W., Nathanson, N. & Hodous, J. Am. J. Epidem. 94, 91–100 (1971).
45.	Anderson, R. M., Whitfield, P. J. & Mills, C. A. J. Anim. Ecol. 46, 550–580 (1977).
46.	Greenwood, M., Bradford-Hill, A., Topley, W. W. C. & Wilson, J. Experimental Epidemiology: Medical Research Council Special Report No. 209 (HMSO, London, 1936).
47.	Greenwood, M. & Topley, W. W. C. J. Hyg. 26, 45–110 (1925).
48.	Fenner, F. J. Immun. 63, 341–373 (1949).
49.	Fenner, F. J. Hyg. 46, 383–393 (1948).
50.	Kermack, W. O. & McKendrick, A. G. Proc. R. Soc. A 115, 700–721 (1927).
51.	Anderson, R. M. Nature 279, 150–152 (1979).
52.	Roitt, I. M. Essential Immunology (Blackwell, Oxford, 1976).
53.	Fox, J. P., Elreback, L., Scott, W., Gatewood, L. & Ackerman, E. Am. J. Epidem. 94, 179–180 (1971).
54.	Stuart-Harris, C. H. in Virus Virulence and Pathogenicity (CIBA Fdn Symp. 4) (Churchill Livingstone, London, 1960).
55.	Deevey, E. S. Scient. Am. 203, 195–207 (1960).
56.	Ehrlich, P. R., Ehrlich, A. H. & Holdren, J. P. Ecoscience: Population, Resources, Environment. Ch. 5 (Freeman, San Francisco, 1977).
57.	Black, F. L. et al. Am. J. Epidem. 100, 230–250 (1974).
58.	Black, F. L. Science 187, 515–518 (1975).
59.	Matumota, M. Bact. Rev. 33, 404–418 (1969).
60.	Nathanson, N., Yorke, J. H., Pianigiani, G. & Matin, J. in Persistent Viruses (eds Stevens, J., Todaro, G. J. & Fox, F. L.) (Academic, New York, 1978).
61.	Tyrell, D. A. J. in Health and Disease in Tribal Societies (CIBA Fdn Symp. 49) (NorthHolland, Amsterdam, 1977).
62.	Bartlett, M. S. J. R. Stat. Soc. A 120, 48–70 (1957).
63.	Bartlett, M. S. J. R. Stat. Soc. A123, 37–44 (1960).
64.	Black, F. L. J. theor. Biol. 11, 207–211 (1966).
65.	London, W. P. & Yorke, J. A. Am. J. Epidem. 98, 453–468 (1973).
66.	Yorke, J. A. & London, W. P. Am. J. Epidem. 98, 469–482 (1973).
67.	Fenner, F. & White, D. O. Medical Virology (Academic, New York, 1970).
68.	Fenner, F., McAuslan, B. R., Mimms, C. A., Sambrook, J. & White, D. O. The Biology of Animal Viruses (Academic, New York, 1974).
69.	Christie, A. B. Infectious Diseases: Epidemiology and Clinical Practice (Churchill Livingstone, London, 1974).
70.	Burnet, M. & White, D. O. Natural History of Infectious Disease (Cambridge University Press, 1972).
71.	Health and Disease in Tribal Societies (CIBA Fdn Symp. 49) (North-Holland, Amsterdam, 1977).
72.	Tanada, Y. in Biological Control of Insect Pests and Weeds (ed. DeBach, P.) (Chapman and Hall, London, 1964).
73.	Bruce-Chwatt, L. J. & Bruce-Chwatt, J. M. Bull. N. Y. Acad. Med. 50, 1069–1080 (1974).
74.	Smith, J. H., Dyck, J. R. & Connor, P. H. Am. J. trop. Med. Hyg. 25, 637–643 (1976).
75.	Ford, J. (ed.) The Role of Trypanosomiasis in African Ecology: A Study of the Tsetse Fly Problem (Oxford University Press, 1971).