Comparison of the transmission efficiency and plague progression dynamics associated with two mechanisms by which fleas transmit Yersinia pestis

Abstract

Yersinia pestis can be transmitted by fleas during the first week after an infectious blood meal, termed early-phase or mass transmission, and again after Y. pestis forms a cohesive biofilm in the flea foregut that blocks normal blood feeding. We compared the transmission efficiency and the progression of infection after transmission by Oropsylla montana fleas at both stages. Fleas were allowed to feed on mice three days after an infectious blood meal to evaluate early-phase transmission, or after they had developed complete proventricular blockage. Transmission was variable and rather inefficient by both modes, and the odds of early-phase transmission was positively associated with the number of infected fleas that fed. Disease progression in individual mice bitten by fleas infected with a bioluminescent strain of Y. pestis was tracked. An early prominent focus of infection at the intradermal flea bite site and dissemination to the draining lymph node(s) soon thereafter were common features, but unlike what has been observed in intradermal injection models, this did not invariably lead to further systemic spread and terminal disease. Several of these mice resolved the infection without progression to terminal sepsis and developed an immune response to Y. pestis, particularly those that received an intermediate number of early-phase flea bites. Furthermore, two distinct types of terminal disease were noted: the stereotypical rapid onset terminal disease within four days, or a prolonged onset preceded by an extended, fluctuating infection of the lymph nodes before eventual systemic dissemination. For both modes of transmission, bubonic plague rather than primary septicemic plague was the predominant disease outcome. The results will help to inform mathematical models of flea-borne plague dynamics used to predict the relative contribution of the two transmission modes to epizootic outbreaks that erupt periodically from the normal enzootic background state.

Oral Sylvatic Plague Vaccine Does Not Adequately Protect Prairie Dogs (Cynomys spp.) for Endangered Black-Footed Ferret (Mustela nigripes) Conservation

“…When assessed in combination, (1) nonvaccinated juveniles, (2) some percentage of the PD population that does not consume bait, (3) some level of less-than-sufficient immune response, (4) incomplete vaccine protection, and (5) time for immunity to develop, a large percentage of the population remains vulnerable to plague for at least 6–7 months each year from April to October. This is a time period in which the most common BTPD flea ( O. hirsuta ) typically increases in abundance (Wilder et al 2008 ), thus increasing plague risk (Lorange et al 2005 , Tripp et al 2009 , Bosio et al 2020 , Eads et al 2020 , Biggins et al 2021b ; although see Brinkerhoff et al 2010 ). The low survival rates observed on vaccine plots during active plague in this study, in Boulerice ( 2017 ) and in Tripp et al ( 2017 ) should not be surprising given these constraints.…”

Plague risk in the western United States over seven decades of environmental change

“…Human cases of plague occur sporadically but consistently in the Western United States, driven partially by exposure to infected cats and dogs that have acquired the infection outside of the home. The vast majority of the human cases in the United States are infected with the bacterium through flea bites (Campbell et al, 2019 ), which typically leads to bubonic plague if the infection is deposited into the skin tissue and results in an infection of the lymphatic system, or (less commonly rarely) as septicemic plague if the infection is deposited in the blood stream (Bosio et al, 2020 ). In only about 3% of the human cases, the disease manifests as pneumonic plague, when the infection was acquired by inhaling infectious droplets coughed up by infected animals or humans (Campbell et al, 2019 ).…”

Antibiotic Therapy of Plague: A Review

“…Hence, the clinical picture is nonspecific, with general organ system failure. Histological and bacteriological analyses have revealed that 10% to 30% of mice bitten by infected fleas succumb to fatal bacteremia without developing a bubo [ 21 , 31 , 32 , 35 ]. Thus, the flea transmits both bubonic plague and primary septicemic plague.…”