Skip to main content
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2000 Nov 7;267(1458):2219–2230. doi: 10.1098/rspb.2000.1272

Bubonic plague: a metapopulation model of a zoonosis.

M J Keeling 1, C A Gilligan 1
PMCID: PMC1690796  PMID: 11413636

Abstract

Bubonic plague (Yersinia pestis) is generally thought of as a historical disease; however, it is still responsible for around 1000-3000 deaths each year worldwide. This paper expands the analysis of a model for bubonic plague that encompasses the disease dynamics in rat, flea and human populations. Some key variables of the deterministic model, including the force of infection to humans, are shown to be robust to changes in the basic parameters, although variation in the flea searching efficiency, and the movement rates of rats and fleas will be considered throughout the paper. The stochastic behaviour of the corresponding metapopulation model is discussed, with attention focused on the dynamics of rats and the force of infection at the local spatial scale. Short-lived local epidemics in rats govern the invasion of the disease and produce an irregular pattern of human cases similar to those observed. However, the endemic behaviour in a few rat subpopulations allows the disease to persist for many years. This spatial stochastic model is also used to identify the criteria for the spread to human populations in terms of the rat density. Finally, the full stochastic model is reduced to the form of a probabilistic cellular automaton, which allows the analysis of a large number of replicated epidemics in large populations. This simplified model enables us to analyse the spatial properties of rat epidemics and the effects of movement rates, and also to test whether the emergent metapopulation behaviour is a property of the local dynamics rather than the precise details of the model.

Full Text

The Full Text of this article is available as a PDF (738.3 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Appleby A. B. The disappearance of plague: a continuing puzzle. Econ Hist Rev. 1980;33(2):161–173. doi: 10.1111/j.1468-0289.1980.tb01821.x. [DOI] [PubMed] [Google Scholar]
  2. Barreto A., Aragon M., Epstein P. R. Bubonic plague outbreak in Mozambique, 1994. Lancet. 1995 Apr 15;345(8955):983–984. doi: 10.1016/s0140-6736(95)90730-0. [DOI] [PubMed] [Google Scholar]
  3. Beard M. L., Maupin G. O., Craven R. B., Montman C. E., Barnes A. M. Laboratory and field trials of permethrin-treated cotton used as nesting material to control fleas (Insecta: Siphonaptera) on cricetid rodents. J Med Entomol. 1992 Mar;29(2):338–342. doi: 10.1093/jmedent/29.2.338. [DOI] [PubMed] [Google Scholar]
  4. Boisier P., Rasolomaharo M., Ranaivoson G., Rasoamanana B., Rakoto L., Andrianirina Z., Andriamahefazafy B., Chanteau S. Urban epidemic of bubonic plague in Majunga, Madagascar: epidemiological aspects. Trop Med Int Health. 1997 May;2(5):422–427. [PubMed] [Google Scholar]
  5. Chanteau S., Ratsifasoamanana L., Rasoamanana B., Rahalison L., Randriambelosoa J., Roux J., Rabeson D. Plague, a reemerging disease in Madagascar. Emerg Infect Dis. 1998 Jan-Mar;4(1):101–104. doi: 10.3201/eid0401.980114. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Craven R. B., Maupin G. O., Beard M. L., Quan T. J., Barnes A. M. Reported cases of human plague infections in the United States, 1970-1991. J Med Entomol. 1993 Jul;30(4):758–761. doi: 10.1093/jmedent/30.4.758. [DOI] [PubMed] [Google Scholar]
  7. Davis R. M. Use of orally administered chitin inhibitor (lufenuron) to control flea vectors of plague on ground squirrels in California. J Med Entomol. 1999 Sep;36(5):562–567. doi: 10.1093/jmedent/36.5.562. [DOI] [PubMed] [Google Scholar]
  8. Dean M. Politics of euthanasia in the UK. Lancet. 1995 Mar 18;345(8951):714–714. doi: 10.1016/s0140-6736(95)90875-7. [DOI] [PubMed] [Google Scholar]
  9. FLEAS and plague. J Trop Med Hyg. 1954 Jan;57(1):1–2. [PubMed] [Google Scholar]
  10. Galimand M., Guiyoule A., Gerbaud G., Rasoamanana B., Chanteau S., Carniel E., Courvalin P. Multidrug resistance in Yersinia pestis mediated by a transferable plasmid. N Engl J Med. 1997 Sep 4;337(10):677–680. doi: 10.1056/NEJM199709043371004. [DOI] [PubMed] [Google Scholar]
  11. Gratz N. G. Emerging and resurging vector-borne diseases. Annu Rev Entomol. 1999;44:51–75. doi: 10.1146/annurev.ento.44.1.51. [DOI] [PubMed] [Google Scholar]
  12. Hinnebusch B. J., Gage K. L., Schwan T. G. Estimation of vector infectivity rates for plague by means of a standard curve-based competitive polymerase chain reaction method to quantify Yersinia pestis in fleas. Am J Trop Med Hyg. 1998 May;58(5):562–569. doi: 10.4269/ajtmh.1998.58.562. [DOI] [PubMed] [Google Scholar]
  13. Keeling M. J. Modelling the persistence of measles. Trends Microbiol. 1997 Dec;5(12):513–518. doi: 10.1016/S0966-842X(97)01147-5. [DOI] [PubMed] [Google Scholar]
  14. Keeling M., Grenfell B. Stochastic dynamics and a power law for measles variability. Philos Trans R Soc Lond B Biol Sci. 1999 Apr 29;354(1384):769–776. doi: 10.1098/rstb.1999.0429. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kimsey S. W., Carpenter T. E., Pappaioanou M., Lusk E. Benefit-cost analysis of bubonic plague surveillance and control at two campgrounds in California, USA. J Med Entomol. 1985 Sep 20;22(5):499–506. doi: 10.1093/jmedent/22.5.499. [DOI] [PubMed] [Google Scholar]
  16. Maupin G. O., Beard M. L., Hinkson G., Barnes A. M., Craven R. B. Studies on the control of plague in the western United States: laboratory trials of six insecticide dust formulations applied to soil for the control of the plague vector Oropsylla montana (Siphonaptera: Ceratophyllidae). J Med Entomol. 1991 Nov;28(6):770–775. doi: 10.1093/jmedent/28.6.770. [DOI] [PubMed] [Google Scholar]
  17. McCormick J. B. Epidemiology of emerging/re-emerging antimicrobial-resistant bacterial pathogens. Curr Opin Microbiol. 1998 Feb;1(1):125–129. doi: 10.1016/s1369-5274(98)80152-5. [DOI] [PubMed] [Google Scholar]
  18. McEvedy C. The bubonic plague. Sci Am. 1988 Feb;258(2):118–123. doi: 10.1038/scientificamerican0288-118. [DOI] [PubMed] [Google Scholar]
  19. Noble J. V. Geographic and temporal development of plagues. Nature. 1974 Aug 30;250(5469):726–729. doi: 10.1038/250726a0. [DOI] [PubMed] [Google Scholar]
  20. doi: 10.1098/rstb.1997.0143. [DOI] [PMC free article] [Google Scholar]
  21. Pinner R. W. Addressing the challenges of emerging infectious disease. Am J Med Sci. 1996 Jan;311(1):3–8. doi: 10.1097/00000441-199601000-00002. [DOI] [PubMed] [Google Scholar]
  22. Risse G. B. "A long pull, a strong pull, and all together": San Francisco and bubonic plague, 1907-1908. Bull Hist Med. 1992 Summer;66(2):260–286. [PubMed] [Google Scholar]
  23. Rosser W. W. Bubonic plague. J Am Vet Med Assoc. 1987 Aug 15;191(4):406–409. [PubMed] [Google Scholar]
  24. SHARIF M. Spread of plague in the southern and central divisions of Bombay Province and plague endemic centers in the Indo-Pakistan subcontinent. Bull World Health Organ. 1951;4(1):75–109. [PMC free article] [PubMed] [Google Scholar]
  25. Scott S., Duncan C. J., Duncan S. R. The plague in Penrith, Cumbria, 1597/8: its causes, biology and consequences. Ann Hum Biol. 1996 Jan-Feb;23(1):1–21. doi: 10.1080/03014469600004232. [DOI] [PubMed] [Google Scholar]
  26. Slack P. The disappearance of plague: an alternative view. Econ Hist Rev. 1981;34(3):469–476. doi: 10.1111/j.1468-0289.1981.tb02081.x. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES