Revisiting the Plasmodium sporozoite inoculum and elucidating the efficiency with which malaria parasites progress through the mosquito

Abstract Malaria is initiated when infected anopheline mosquitoes inoculate sporozoites as they probe for blood. It is thought that all infected mosquitoes are equivalent in terms of their infectious potential, with parasite burden having no role in transmission success. In this study, using mosquit...

Full description

Bibliographic Details
Main Authors: Sachie Kanatani, Deborah Stiffler, Teun Bousema, Gayane Yenokyan, Photini Sinnis
Format: Article
Language:English
Published: Nature Portfolio 2024-01-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-44962-4
_version_ 1797276459011670016
author Sachie Kanatani
Deborah Stiffler
Teun Bousema
Gayane Yenokyan
Photini Sinnis
author_facet Sachie Kanatani
Deborah Stiffler
Teun Bousema
Gayane Yenokyan
Photini Sinnis
author_sort Sachie Kanatani
collection DOAJ
description Abstract Malaria is initiated when infected anopheline mosquitoes inoculate sporozoites as they probe for blood. It is thought that all infected mosquitoes are equivalent in terms of their infectious potential, with parasite burden having no role in transmission success. In this study, using mosquitoes harboring the entire range of salivary gland sporozoite loads observed in the field, we demonstrate a strong and highly significant correlation between mosquito parasite burden and inoculum size. We then link the inoculum data to oocyst counts, the most commonly-used metric to assess mosquito infection in the field, and determine the efficiency with which oocyst sporozoites enter mosquito salivary glands. Taken together our data support the conclusion that mosquitoes with higher parasite burdens are more likely to initiate infection and contribute to onward transmission. Overall these data may account for some of the unexplained heterogeneity in transmission and enable more precise benchmarks for transmission-blocking interventions.
first_indexed 2024-03-07T15:28:31Z
format Article
id doaj.art-36d12afc8d644f59bbdf13589a8d3cb6
institution Directory Open Access Journal
issn 2041-1723
language English
last_indexed 2024-03-07T15:28:31Z
publishDate 2024-01-01
publisher Nature Portfolio
record_format Article
series Nature Communications
spelling doaj.art-36d12afc8d644f59bbdf13589a8d3cb62024-03-05T16:34:20ZengNature PortfolioNature Communications2041-17232024-01-0115111310.1038/s41467-024-44962-4Revisiting the Plasmodium sporozoite inoculum and elucidating the efficiency with which malaria parasites progress through the mosquitoSachie Kanatani0Deborah Stiffler1Teun Bousema2Gayane Yenokyan3Photini Sinnis4Department of Molecular Microbiology & Immunology, Johns Hopkins Bloomberg School of Public HealthDepartment of Molecular Microbiology & Immunology, Johns Hopkins Bloomberg School of Public HealthDepartment of Medical Microbiology & Radboud Center for Infectious Diseases, Radboud University Medical CenterDepartment of Biostatistics, Johns Hopkins Bloomberg School of Public HealthDepartment of Molecular Microbiology & Immunology, Johns Hopkins Bloomberg School of Public HealthAbstract Malaria is initiated when infected anopheline mosquitoes inoculate sporozoites as they probe for blood. It is thought that all infected mosquitoes are equivalent in terms of their infectious potential, with parasite burden having no role in transmission success. In this study, using mosquitoes harboring the entire range of salivary gland sporozoite loads observed in the field, we demonstrate a strong and highly significant correlation between mosquito parasite burden and inoculum size. We then link the inoculum data to oocyst counts, the most commonly-used metric to assess mosquito infection in the field, and determine the efficiency with which oocyst sporozoites enter mosquito salivary glands. Taken together our data support the conclusion that mosquitoes with higher parasite burdens are more likely to initiate infection and contribute to onward transmission. Overall these data may account for some of the unexplained heterogeneity in transmission and enable more precise benchmarks for transmission-blocking interventions.https://doi.org/10.1038/s41467-024-44962-4
spellingShingle Sachie Kanatani
Deborah Stiffler
Teun Bousema
Gayane Yenokyan
Photini Sinnis
Revisiting the Plasmodium sporozoite inoculum and elucidating the efficiency with which malaria parasites progress through the mosquito
Nature Communications
title Revisiting the Plasmodium sporozoite inoculum and elucidating the efficiency with which malaria parasites progress through the mosquito
title_full Revisiting the Plasmodium sporozoite inoculum and elucidating the efficiency with which malaria parasites progress through the mosquito
title_fullStr Revisiting the Plasmodium sporozoite inoculum and elucidating the efficiency with which malaria parasites progress through the mosquito
title_full_unstemmed Revisiting the Plasmodium sporozoite inoculum and elucidating the efficiency with which malaria parasites progress through the mosquito
title_short Revisiting the Plasmodium sporozoite inoculum and elucidating the efficiency with which malaria parasites progress through the mosquito
title_sort revisiting the plasmodium sporozoite inoculum and elucidating the efficiency with which malaria parasites progress through the mosquito
url https://doi.org/10.1038/s41467-024-44962-4
work_keys_str_mv AT sachiekanatani revisitingtheplasmodiumsporozoiteinoculumandelucidatingtheefficiencywithwhichmalariaparasitesprogressthroughthemosquito
AT deborahstiffler revisitingtheplasmodiumsporozoiteinoculumandelucidatingtheefficiencywithwhichmalariaparasitesprogressthroughthemosquito
AT teunbousema revisitingtheplasmodiumsporozoiteinoculumandelucidatingtheefficiencywithwhichmalariaparasitesprogressthroughthemosquito
AT gayaneyenokyan revisitingtheplasmodiumsporozoiteinoculumandelucidatingtheefficiencywithwhichmalariaparasitesprogressthroughthemosquito
AT photinisinnis revisitingtheplasmodiumsporozoiteinoculumandelucidatingtheefficiencywithwhichmalariaparasitesprogressthroughthemosquito