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Poor vector competence of the human flea, Pulex irritans, to transmit Yersinia pestis

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...

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Autores principales: Miarinjara, Adélaïde, Bland, David M., Belthoff, James R., Hinnebusch, B. Joseph
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8194109/
https://www.ncbi.nlm.nih.gov/pubmed/34112224
http://dx.doi.org/10.1186/s13071-021-04805-3
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author Miarinjara, Adélaïde
Bland, David M.
Belthoff, James R.
Hinnebusch, B. Joseph
author_facet Miarinjara, Adélaïde
Bland, David M.
Belthoff, James R.
Hinnebusch, B. Joseph
author_sort Miarinjara, Adélaïde
collection PubMed
description 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 × 10(8) to 1 × 10(9) 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: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-021-04805-3.
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spelling pubmed-81941092021-06-15 Poor vector competence of the human flea, Pulex irritans, to transmit Yersinia pestis Miarinjara, Adélaïde Bland, David M. Belthoff, James R. Hinnebusch, B. Joseph Parasit Vectors Research 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 × 10(8) to 1 × 10(9) 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: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-021-04805-3. BioMed Central 2021-06-10 /pmc/articles/PMC8194109/ /pubmed/34112224 http://dx.doi.org/10.1186/s13071-021-04805-3 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Miarinjara, Adélaïde
Bland, David M.
Belthoff, James R.
Hinnebusch, B. Joseph
Poor vector competence of the human flea, Pulex irritans, to transmit Yersinia pestis
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 Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8194109/
https://www.ncbi.nlm.nih.gov/pubmed/34112224
http://dx.doi.org/10.1186/s13071-021-04805-3
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