Scientists have long been puzzled how the bubonic plague bacteria, Yersinia pestis, can cause both stable, enzootic disease among rodents, as well as sudden, lethal epizootic outbreaks that decimate the same rodent populations. A new study concludes that the difference might relate to the fleas that carry Y. pestis between animals. Fleas with only early-phase infection are insufficient to drive an epizootic among most wild rodents, and favor a more stable enzootic state, according to the research published this week in PLOS Pathogens by Joseph Hinnebusch of the National Institute of Allergy and Infections Diseases Rocky Mountain Laboratories, U.S., and colleagues.
Plague primarily afflicts rodents, including rats, mice, gerbils, squirrels, marmots and prairie dogs. The bacteria circulate within these host populations through several flea vector species. Fleas can transmit Y. pestis in different stages following an infectious blood meal; transmission can occur the very next time they feed, a phenomenon referred to as early-phase transmission. Later, “blockage-dependent transmission” occurs after Y. pestis forms a bacterial biofilm in the fleas’ digestive systems, blocking the flow of an incoming meal and causing blood to recoil back into the bite site after mixing with the biofilm.
In the new study, researchers for the first time empirically evaluated the relative efficiency of the different phases of transmission by individual fleas. Cohorts of a ground squirrel flea, Oropsylla montana, were infected by feeding on mouse or rat blood infected with Y. pestis. Transmission efficiency of individual O. montana fleas was then measured over a four-week period and the researchers created models to show how this efficiency would translate to the spread of Y. pestis through a rodent population.
The results indicated that blockage-dependent transmission is much more efficient than early-phase transmission, in terms of the probability of transmission, the number of bacteria transmitted, and the capability of driving an epizootic outbreak. Early-phase transmission, the models showed, could drive an epizootic only in naïve, very susceptible host populations and when the flea burden is high. Moreover, the low dose of bacteria typically transmitted in early-phase transmission may “immunize” many individuals, acting to promote an enzootic state.
“Our models suggest that exposure of most wild rodents to sublethal, immunizing doses of Y. pestis transmitted during the early phase may ameliorate rapid epizootic spread by reducing the number of susceptible individuals in the population,” the authors say. “In many situations early-phase transmission may be more important in maintaining the enzootic state than in driving an epizootic.”
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