Host Resistance, Population Structure and the Long-Term Persistence of Bubonic Plague: Contributions of a Modelling Approach in the Malagasy Focus
Open Access
- 9 May 2013
- journal article
- research article
- Published by Public Library of Science (PLoS) in PLOS Computational Biology
- Vol. 9 (5) , e1003039
Abstract
Although bubonic plague is an endemic zoonosis in many countries around the world, the factors responsible for the persistence of this highly virulent disease remain poorly known. Classically, the endemic persistence of plague is suspected to be due to the coexistence of plague resistant and plague susceptible rodents in natural foci, and/or to a metapopulation structure of reservoirs. Here, we test separately the effect of each of these factors on the long-term persistence of plague. We analyse the dynamics and equilibria of a model of plague propagation, consistent with plague ecology in Madagascar, a major focus where this disease is endemic since the 1920s in central highlands. By combining deterministic and stochastic analyses of this model, and including sensitivity analyses, we show that (i) endemicity is favoured by intermediate host population sizes, (ii) in large host populations, the presence of resistant rats is sufficient to explain long-term persistence of plague, and (iii) the metapopulation structure of susceptible host populations alone can also account for plague endemicity, thanks to both subdivision and the subsequent reduction in the size of subpopulations, and extinction-recolonization dynamics of the disease. In the light of these results, we suggest scenarios to explain the localized presence of plague in Madagascar. Bubonic plague, known to have marked human history by three deadly pandemics, is an infectious disease which mainly circulates in wild rodent populations and is transmitted by fleas. Although this disease can be quickly lethal to its host, it has persisted on long-term in many rodent populations around the world. The reasons for this persistence remain poorly known. Two mechanisms have been invoked, but not yet explicitly and independently tested: first, the spatial structure of rodent populations (subdivision into several subpopulations) and secondly, the presence of, not only plague-susceptible rodents, but also plague-resistant ones. To gain insight into the role of the above two factors in plague persistence, we analysed a mathematical model of plague propagation. We applied our analyses to the case of Madagascar, where plague has persisted on central highlands since the 1920s and is responsible for about 30% of the human cases worldwide. We found that the long-term persistence of plague can be explained by the presence of any of the above two factors. These results allowed us to propose scenarios to explain the localized presence of plague in the Malagasy highlands, and help understand the persistence of plague in many wild foci.Keywords
This publication has 61 references indexed in Scilit:
- Phylogeography and Molecular Epidemiology of Yersinia pestis in MadagascarPLOS Neglected Tropical Diseases, 2011
- Emergence, spread, persistence and fade-out of sylvatic plague in KazakhstanProceedings Of The Royal Society B-Biological Sciences, 2011
- Plague outbreaks in prairie dog populations explained by percolation thresholds of alternate host abundanceProceedings of the National Academy of Sciences, 2010
- Disease Limits Populations: Plague and Black-Tailed Prairie DogsVector-Borne and Zoonotic Diseases, 2010
- Next-generation tools for evolutionary invasion analysesJournal of The Royal Society Interface, 2009
- Mapping the Spread of Malaria Drug ResistancePLOS Medicine, 2009
- Plague metapopulation dynamics in a natural reservoir: the burrow system as the unit of studyEpidemiology and Infection, 2006
- Classic flea-borne transmission does not drive plague epizootics in prairie dogsProceedings of the National Academy of Sciences, 2006
- Poor Vector Competence of Fleas and the Evolution of Hypervirulence inYersinia pestisThe Journal of Infectious Diseases, 2005
- Exact stochastic simulation of coupled chemical reactionsThe Journal of Physical Chemistry, 1977