Sylvatic Plague Studies: II. The Fate of Pasteurella Pestis in the Flea

Douglas, J. R.; Wheeler, C. M.

doi:10.1093/infdis/72.1.18

Cited by 43 publications

(46 citation statements)

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“…Therefore, the host-flea couple could not support anything more than a very transient epizootic. Nevertheless, O. montana is important in amplifying plague and particularly in transmitting it to humans, because this flea aggressively seeks new hosts, including humans, when its preferred host dies (Douglas and Wheeler, 1943;Holdenreid, 1952;Quan et al, 1960;Nelson, 1980;Barnes, 1982;Gage and Kosoy, 2005).…”

Section: Rodentmentioning

confidence: 99%

Modeling Plague Persistence in Host-Vector Communities in California

Foley¹,

Zipser²,

Chomel³

et al. 2007

Journal of Wildlife Diseases

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ABSTRACT:Plague is an enzootic disease in the western United States, even though long-term persistent infections do not seem to occur. Enzootic persistence may occur as a function of dynamic interactions between flea vectors and transiently infected hosts, but the specific levels of vector competence, host competence, and transmission and recovery rates that would promote persistence and emergence among wild hosts and vectors are not known. We developed a mathematical model of enzootic plague in the western United States and implemented the model with the following objectives: 1) to use matrix manipulation within a classic susceptibleRinfectiveRresistantRsusceptible (SIRS) model framework to describe transmission of the plague bacterium Yersinia pestis among rodents and fleas in California, 2) to perform sensitivity analysis with model parameters and variables to indicate which values tended to dominate model output, and 3) to determine whether enzootic maintenance would be predicted with realistic parameter values obtained from the literature for Y. pestis in California rodents and fleas. The model PlagueSIRS was implemented in discrete time as a computer simulation incorporating environmental stochasticity and seasonality, by using matrix functions in the computer language R, allowing any number of rodent and flea species to interact through parasitism and disease transmission. Sensitivity analysis indicated that the model was sensitive to flea attack rate, host recovery rate, and rodent host carrying capacity but relatively insensitive to changes in the duration of latent infection in the flea, host and vector competence, flea recovery from infection, and host mortality attributable to plague. Realistic parameters and variable values did allow for the model to predict enzootic plague in some combinations, specifically when rodent species that were susceptible to infection but resistant to morbidity were parasitized by multiple poorly competent flea species, including some that were present year-round. This model could be extended to similar vectorborne disease systems and could be used iteratively with data collection in sylvatic plague studies to better understand plague persistence and emergence in nature.

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Section: Rodentmentioning

confidence: 99%

Modeling Plague Persistence in Host-Vector Communities in California

Foley¹,

Zipser²,

Chomel³

et al. 2007

Journal of Wildlife Diseases

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“…25,27,28 Previous studies suggest that fleas imbibe up to 0.5 L of blood during each feeding, depending on sex and species. 29 If an individual flea ingests 0.5 L of blood with 10 7 -10 8 bacteria/mL, it will be infected with approximately 10 3 -10 4 bacteria immediately after feeding. Ingesting smaller quantities of Y. pestis results in inconsistent infection and/or inability to transmit at a later time.…”

Section: Preparation Of Y Pestis Cells Expressing Green Fluorescent mentioning

confidence: 99%

Quantitative competitive PCR as a technique for exploring flea-Yersina pestis dynamics.

Engelthaler

Hinnebusch²,

Rittner³

et al. 2000

The American Journal of Tropical Medicine and Hygiene

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Abstract. We used a quantitative competitive polymerase chain reaction assay to quantify Yersinia pestis loads in fleas and bacteremia levels in mice that were used as sources of infectious blood meals for feeding the fleas. Xenopsylla cheopis, the Oriental rat flea, achieved higher infection rates, developed greater bacterial loads, and became infectious more rapidly than Oropsylla montana, a ground squirrel flea. Both flea species required about 10 6 Y. pestis cells per flea to be able to transmit to mice. Most fleas that achieved these levels, however, were incapable of transmitting. Our results suggest that at the time of flea feeding, host blood must contain Ն10 6 bacteria/ml to result in detectable Y. pestis infections in these fleas, and Ն10 7 bacteria/mL to cause infection levels sufficient for both species to eventually become capable of transmitting Y. pestis to uninfected mice. Yersinia pestis colonies primarily developed in the midguts of O. montana, whereas infections in X. cheopis often developed simultaneously in the proventriculus and the midgut. These findings were visually confirmed by infecting fleas with a strain of Y. pestis that had been transformed with the green fluorescent protein gene.

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“…Fleas take small blood meals (0.1-0.3 μl), so Y. pestis must achieve a level of >10 7 per milliliter in the peripheral blood in order to have a 50% chance of infecting its vector. Bacteremias of 10 8 to 10 9 per milliliter are routinely present in moribund white laboratory mice (Douglas and Wheeler, 1943). The concept of a very high threshold level of bacteremia, below which infection of feeding fleas does not occur or is rare, is supported by the observations of several investigators (Douglas and Wheeler, 1943;Pollitzer, 1954;Kartman and Quan, 1964).…”

Section: Coevolution Of Flea-borne Transmission and Increased Virulenmentioning

confidence: 99%

“…Bacteremias of 10 8 to 10 9 per milliliter are routinely present in moribund white laboratory mice (Douglas and Wheeler, 1943). The concept of a very high threshold level of bacteremia, below which infection of feeding fleas does not occur or is rare, is supported by the observations of several investigators (Douglas and Wheeler, 1943;Pollitzer, 1954;Kartman and Quan, 1964). Thus, Y. pestis does not infect the flea very efficiently in the first place, and this would have been strong selective pressure favoring more invasive, and consequently, more virulent strains able to produce the severe bacteremia that typifies plague.…”

Section: Coevolution Of Flea-borne Transmission and Increased Virulenmentioning

confidence: 99%

The Evolution of Flea-borne Transmission inYersinia pestis

Hinnebusch

2005

Current Issues in Molecular Biology

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Transmission by fleabite is a recent evolutionary adaptation that distinguishes Yersinia pestis, the agent of plague, from Yersinia pseudotuberculosis and all other enteric bacteria. The very close genetic relationship between Y. pestis and Y. pseudotuberculosis indicates that just a few discrete genetic changes were sufficient to give rise to fleaborne transmission. Y. pestis exhibits a distinct infection phenotype in its flea vector, and a transmissible infection depends on genes that are specifically required in the flea, but not the mammal. Transmission factors identified to date suggest that the rapid evolutionary transition of Y. pestis to flea-borne transmission within the last 1,500 to 20,000 years involved at least three steps: acquisition of the two Y. pestis-specific plasmids by horizontal gene transfer; and recruitment of endogenous chromosomal genes for new functions. Perhaps reflective of the recent adaptation, transmission of Y. pestis by fleas is inefficient, and this likely imposed selective pressure favoring the evolution of increased virulence in this pathogen. IntroductionPathogenic bacteria must overcome several physiological and immunological challenges to successfully infect even a single type of host, such as a mammal. It is remarkable, then, that bacteria transmitted by blood-feeding arthropods are capable of infecting two very different hosts during their life cycle: an invertebrate (usually an insect or tick) and a mammal. As if this were not enough of a challenge, it is not sufficient that an arthropod-borne bacterium successfully infect both vector and host. It must establish a transmissible infection in both; that is, it must infect the vector in such a way as to be transmitted during a blood meal, and it must infect the mammal in a way that allows uptake by a blood-feeding arthropod. This feat of evolution has occurred relatively rarely, but nonetheless arthropod-borne transmission has developed independently in a phylogenetically diverse group of microorganisms, including the rickettsiae, spirochetes in the genus Borrelia, and the Gram-negative bacteria.Compared to the ancient relationship of rickettsiae and spirochetes with arthropods, the vector relationship between Y. pestis and fleas is new. Population genetics and comparative genomics analyses indicate that Y. pestis is a clonal variant of Y. pseudotuberculosis that diverged only within the last 1,500 to 20,000 years (Achtman et Hinchcliffe et al., 2003;Chain et al., 2004). Presumably, the change from the food-and water-borne transmission of the Y. pseudotuberculosis ancestor to the flea-borne transmission of Y. pestis occurred during this evolutionarily short period of time. The monophyletic relationship of these two sister-species implies that the genetic changes that underlie the ability of Y. pestis to use the flea for its transmission vector are relatively few and discrete. Therefore, the Y. pseudotuberculosis -Y. pestis species complex provides an interesting case study in the evolution of arthropod-borne transm...

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Sylvatic Plague Studies: II. The Fate of Pasteurella Pestis in the Flea

Cited by 43 publications

References 0 publications

Modeling Plague Persistence in Host-Vector Communities in California

Modeling Plague Persistence in Host-Vector Communities in California

Quantitative competitive PCR as a technique for exploring flea-Yersina pestis dynamics.

The Evolution of Flea-borne Transmission inYersinia pestis

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