Plague Transmission Models

Transmission of Y. pestis by fleas can occur by at least three different mechanisms, which may be more or less important among the many different species of flea vectors and at different epizootiologic stages. The first is simple mechanical transmission, which can occur if a flea feeds on a new host shortly after taking a blood meal from a highly septicemic host. Mechanical transmission is akin to dirty-needle transmission, in which the inoculum derives from a residue on the flea mouthparts that remains from a prior infected blood meal (Burroughs 1947). Biological transmission, in contrast, is dependent on bacterial multiplication in the flea midgut and subsequent regurgitation into the bite site. The general mechanism of biological transmission was described by the English medical entomologist A. W. Bacot in two classic papers (Bacot and Martin 1914; Bacot 1915). Bacot observed that Y. pestis grew in the form of large aggregates in the midgut of infected fleas and that in some fleas bacterial aggregates also developed in the lumen of the proventriculus, a valve connecting the esophagus and midgut that opens and closes rhythmically during blood feeding. Colonization of the proven-triculus was found to be critical for efficient transmission. As the Y. pestis aggregates grew in the proventriculus, they interfered with its valvular function, permitting regurgitation of blood, carrying bacteria from the midgut or the proven-triculus along with it, back into the bite site. In some fleas, consolidation of the Y. pestis aggregate filled the entire lumen of the proventriculus and completely blocked the passage of blood (Fig. 1). However, complete blockage is not essential for efficient transmission; Bacot thought that incompletely blocked fleas might actually be better transmitters (Bacot 1915). This is often overlooked due to the emphasis on blocked fleas, but is an important component of the classic Bacot model because complete proventricular blockage may not develop regularly in all flea vector species (Bacot 1915; Burroughs 1947; Pollitzer 1954). An alternative

  1. 1 Y. pestis biofilm in the flea. Digestive tract dissected from an X. cheopis flea blocked with a dense biofilm consisting of dark masses of Y. pestis embedded in a paler, viscous ECM (arrows). The contiguous biofilm fills the proventriculus (PV) and extends posteriorly into the lumen of the midgut (MG). E, esophagus
  2. 1 Y. pestis biofilm in the flea. Digestive tract dissected from an X. cheopis flea blocked with a dense biofilm consisting of dark masses of Y. pestis embedded in a paler, viscous ECM (arrows). The contiguous biofilm fills the proventriculus (PV) and extends posteriorly into the lumen of the midgut (MG). E, esophagus type of regurgitative transmission that may not involve bacterial interference of proventricular function was recently described for the squirrel flea Oropsylla montana , which likely contributes to the vector competence of fleas in which proventricular blockage is infrequently observed (Eisen et al. 2006; Webb et al. 2006). Whether this newly described mechanism depends on biofilm formation or is closer to simple mechanical transmission remains to be determined.
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