Poor vector competence of the human flea, Pulex irritans, to transmit Yersinia pestis
Abstract Background 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, although its high prevalence in plague-endemic regions and the presence of infected fleas of this...
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| Format: | Article |
| Language: | English |
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BMC
2021-06-01
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| Series: | Parasites & Vectors |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s13071-021-04805-3 |
| _version_ | 1819007089177001984 |
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| author | Adélaïde Miarinjara David M. Bland James R. Belthoff B. Joseph Hinnebusch |
| author_facet | Adélaïde Miarinjara David M. Bland James R. Belthoff B. Joseph Hinnebusch |
| author_sort | Adélaïde Miarinjara |
| collection | DOAJ |
| description | Abstract Background 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, 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. Methods Wild-caught fleas were maintained in the laboratory and infected by allowing them to feed on human or rat blood containing 2 × 108 to 1 × 109 Y. 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. Results P. 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. Conclusions Our 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 |
| first_indexed | 2024-12-21T00:19:02Z |
| format | Article |
| id | doaj.art-82484b2637ba42ae9973e92256b3afd3 |
| institution | Directory Open Access Journal |
| issn | 1756-3305 |
| language | English |
| last_indexed | 2024-12-21T00:19:02Z |
| publishDate | 2021-06-01 |
| publisher | BMC |
| record_format | Article |
| series | Parasites & Vectors |
| spelling | doaj.art-82484b2637ba42ae9973e92256b3afd32022-12-21T19:22:09ZengBMCParasites & Vectors1756-33052021-06-0114111510.1186/s13071-021-04805-3Poor vector competence of the human flea, Pulex irritans, to transmit Yersinia pestisAdélaïde Miarinjara0David M. Bland1James R. Belthoff2B. Joseph Hinnebusch3Laboratory of Bacteriology, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, NIHLaboratory of Bacteriology, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, NIHDepartment of Biological Sciences, Boise State UniversityLaboratory of Bacteriology, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, NIHAbstract Background 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, 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. Methods Wild-caught fleas were maintained in the laboratory and infected by allowing them to feed on human or rat blood containing 2 × 108 to 1 × 109 Y. 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. Results P. 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. Conclusions Our 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 abstracthttps://doi.org/10.1186/s13071-021-04805-3Pulex irritansYersinia pestisFleaPlagueTransmission |
| spellingShingle | Adélaïde Miarinjara David M. Bland James R. Belthoff B. Joseph Hinnebusch Poor vector competence of the human flea, Pulex irritans, to transmit Yersinia pestis Parasites & Vectors Pulex irritans Yersinia pestis Flea Plague Transmission |
| title | Poor vector competence of the human flea, Pulex irritans, to transmit Yersinia pestis |
| title_full | Poor vector competence of the human flea, Pulex irritans, to transmit Yersinia pestis |
| title_fullStr | Poor vector competence of the human flea, Pulex irritans, to transmit Yersinia pestis |
| title_full_unstemmed | Poor vector competence of the human flea, Pulex irritans, to transmit Yersinia pestis |
| title_short | Poor vector competence of the human flea, Pulex irritans, to transmit Yersinia pestis |
| title_sort | poor vector competence of the human flea pulex irritans to transmit yersinia pestis |
| topic | Pulex irritans Yersinia pestis Flea Plague Transmission |
| url | https://doi.org/10.1186/s13071-021-04805-3 |
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