Abstract
BackgroundThe human flea, Pulex irritans, is widespread globally and has a long association with humans, one of its principal hosts. Its role in plague transmission is still under discussion, although its high prevalence in plague-endemic regions and the presence of infected fleas of this species during plague outbreaks has led to proposals that it has been a significant vector in human-to-human transmission in some historical and present-day epidemiologic situations. However, based on a limited number of studies, P. irritans is considered to be a poor vector and receives very little attention from public health policymakers. In this study we examined the vector competence of P. irritans collected from foxes and owls in the western United States, using a standard protocol and artificial infection system.MethodsWild-caught fleas were maintained in the laboratory and infected by allowing them to feed on human or rat blood containing 2 × 108 to 1 × 109Y. pestis/ml. The fleas were then monitored periodically for infection rate and bacterial load, mortality, feeding rate, bacterial biofilm formation in the foregut (proventricular blockage), and ability to transmit Y. pestis after their single infectious blood meal.ResultsP. irritans were susceptible to infection, with more than 30% maintaining high bacterial loads for up to 20 days. Transmission during this time was infrequent and inefficient, however. Consistent with previous studies, a low level of early-phase transmission (3 days after the infectious blood meal) was detected in some trials. Transmission at later time points was also sporadic, and the incidence of proventricular blockage, required for this mode of transmission, was low in fleas infected using rat blood and never occurred in fleas infected using human blood. The highest level of blockage and transmission was seen in fleas infected using rat blood and allowed to feed intermittently rather than daily, indicating that host blood and feeding frequency influence vector competence.ConclusionsOur results affirm the reputation of P. irritans as a feeble vector compared to rodent flea species examined similarly, and its vector competence may be lower when infected by feeding on bacteremic human blood.Graphic abstract
Highlights
The human flea, Pulex irritans, is widespread globally and has a long association with humans, one of its principal hosts
Fleas collected from burrowing owls and foxes were verified as Pulex irritans by standard classification keys based on morphology [46]
Our results substantiate the reputation of P. irritans as a poor and unreliable vector of Y. pestis, after feeding on bacteremic human blood
Summary
The human flea, Pulex irritans, is widespread globally and has a long association with humans, one of its principal hosts. Its role in plague transmission is still under discussion, its high prevalence in plagueendemic regions and the presence of infected fleas of this species during plague outbreaks has led to proposals that it has been a significant vector in human-to-human transmission in some historical and present-day epidemiologic situations. Transmission can occur after the bacteria form a cohesive biofilm in the proventriculus, a valve in the flea foregut that regulates blood flow between the esophagus and midgut during. In a second mode of transmission, fleas can transmit within the first few days after having fed on a host with high-density bacteremia, when they feed on a naïve host [8, 11, 12]. Referred to as mass transmission, because it rarely occurs unless several infected fleas feed simultaneously on a naïve host, it has been recently reexamined and termed early-phase transmission [13]. Early-phase transmission does not require the formation of a mature biofilm, and occurs via regurgitation from a heavily colonized proventriculus [14,15,16,17]
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