Co-infection of the four major Plasmodium species: Effects on densities and gametocyte carriage.

Background Co-infection of the four major species of human malaria parasite Plasmodium falciparum (Pf), P. vivax (Pv), P. malariae (Pm), and P. ovale sp. (Po) is regularly observed, but there is limited understanding of between-species interactions. In particular, little is known about the effects o...

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Published in:PLOS Neglected Tropical Diseases
Main Authors: Aurel Holzschuh, Maria Gruenberg, Natalie E Hofmann, Rahel Wampfler, Benson Kiniboro, Leanne J Robinson, Ivo Mueller, Ingrid Felger, Michael T White
Format: Article in Journal/Newspaper
Language:English
Published: Public Library of Science (PLoS) 2022
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Online Access:https://doi.org/10.1371/journal.pntd.0010760
https://doaj.org/article/cb7ba1da20224a2f805c1d15eddb6829
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spelling ftdoajarticles:oai:doaj.org/article:cb7ba1da20224a2f805c1d15eddb6829 2023-05-15T15:15:16+02:00 Co-infection of the four major Plasmodium species: Effects on densities and gametocyte carriage. Aurel Holzschuh Maria Gruenberg Natalie E Hofmann Rahel Wampfler Benson Kiniboro Leanne J Robinson Ivo Mueller Ingrid Felger Michael T White 2022-09-01T00:00:00Z https://doi.org/10.1371/journal.pntd.0010760 https://doaj.org/article/cb7ba1da20224a2f805c1d15eddb6829 EN eng Public Library of Science (PLoS) https://doi.org/10.1371/journal.pntd.0010760 https://doaj.org/toc/1935-2727 https://doaj.org/toc/1935-2735 1935-2727 1935-2735 doi:10.1371/journal.pntd.0010760 https://doaj.org/article/cb7ba1da20224a2f805c1d15eddb6829 PLoS Neglected Tropical Diseases, Vol 16, Iss 9, p e0010760 (2022) Arctic medicine. Tropical medicine RC955-962 Public aspects of medicine RA1-1270 article 2022 ftdoajarticles https://doi.org/10.1371/journal.pntd.0010760 2022-12-30T23:29:01Z Background Co-infection of the four major species of human malaria parasite Plasmodium falciparum (Pf), P. vivax (Pv), P. malariae (Pm), and P. ovale sp. (Po) is regularly observed, but there is limited understanding of between-species interactions. In particular, little is known about the effects of multiple Plasmodium species co-infections on gametocyte production. Methods We developed molecular assays for detecting asexual and gametocyte stages of Pf, Pv, Pm, and Po. This is the first description of molecular diagnostics for Pm and Po gametocytes. These assays were implemented in a unique epidemiological setting in Papua New Guinea with sympatric transmission of all four Plasmodium species permitting a comprehensive investigation of species interactions. Findings The observed frequency of Pf-Pv co-infection for asexual parasites (14.7%) was higher than expected from individual prevalence rates (23.8%Pf x 47.4%Pv = 11.3%). The observed frequency of co-infection with Pf and Pv gametocytes (4.6%) was higher than expected from individual prevalence rates (13.1%Pf x 28.2%Pv = 3.7%). The excess risk of co-infection was 1.38 (95% confidence interval (CI): 1.09, 1.67) for all parasites and 1.37 (95% CI: 0.95, 1.79) for gametocytes. This excess co-infection risk was partially attributable to malaria infections clustering in some villages. Pf-Pv-Pm triple infections were four times more frequent than expected by chance alone, which could not be fully explained by infections clustering in highly exposed individuals. The effect of co-infection on parasite density was analyzed by systematic comparison of all pairwise interactions. This revealed a significant 6.57-fold increase of Pm density when co-infected with Pf. Pm gametocytemia also increased with Pf co-infection. Conclusions Heterogeneity in exposure to mosquitoes is a key epidemiological driver of Plasmodium co-infection. Among the four co-circulating parasites, Pm benefitted most from co-infection with other species. Beyond this, no general prevailing pattern of ... Article in Journal/Newspaper Arctic Directory of Open Access Journals: DOAJ Articles Arctic PLOS Neglected Tropical Diseases 16 9 e0010760
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic Arctic medicine. Tropical medicine
RC955-962
Public aspects of medicine
RA1-1270
spellingShingle Arctic medicine. Tropical medicine
RC955-962
Public aspects of medicine
RA1-1270
Aurel Holzschuh
Maria Gruenberg
Natalie E Hofmann
Rahel Wampfler
Benson Kiniboro
Leanne J Robinson
Ivo Mueller
Ingrid Felger
Michael T White
Co-infection of the four major Plasmodium species: Effects on densities and gametocyte carriage.
topic_facet Arctic medicine. Tropical medicine
RC955-962
Public aspects of medicine
RA1-1270
description Background Co-infection of the four major species of human malaria parasite Plasmodium falciparum (Pf), P. vivax (Pv), P. malariae (Pm), and P. ovale sp. (Po) is regularly observed, but there is limited understanding of between-species interactions. In particular, little is known about the effects of multiple Plasmodium species co-infections on gametocyte production. Methods We developed molecular assays for detecting asexual and gametocyte stages of Pf, Pv, Pm, and Po. This is the first description of molecular diagnostics for Pm and Po gametocytes. These assays were implemented in a unique epidemiological setting in Papua New Guinea with sympatric transmission of all four Plasmodium species permitting a comprehensive investigation of species interactions. Findings The observed frequency of Pf-Pv co-infection for asexual parasites (14.7%) was higher than expected from individual prevalence rates (23.8%Pf x 47.4%Pv = 11.3%). The observed frequency of co-infection with Pf and Pv gametocytes (4.6%) was higher than expected from individual prevalence rates (13.1%Pf x 28.2%Pv = 3.7%). The excess risk of co-infection was 1.38 (95% confidence interval (CI): 1.09, 1.67) for all parasites and 1.37 (95% CI: 0.95, 1.79) for gametocytes. This excess co-infection risk was partially attributable to malaria infections clustering in some villages. Pf-Pv-Pm triple infections were four times more frequent than expected by chance alone, which could not be fully explained by infections clustering in highly exposed individuals. The effect of co-infection on parasite density was analyzed by systematic comparison of all pairwise interactions. This revealed a significant 6.57-fold increase of Pm density when co-infected with Pf. Pm gametocytemia also increased with Pf co-infection. Conclusions Heterogeneity in exposure to mosquitoes is a key epidemiological driver of Plasmodium co-infection. Among the four co-circulating parasites, Pm benefitted most from co-infection with other species. Beyond this, no general prevailing pattern of ...
format Article in Journal/Newspaper
author Aurel Holzschuh
Maria Gruenberg
Natalie E Hofmann
Rahel Wampfler
Benson Kiniboro
Leanne J Robinson
Ivo Mueller
Ingrid Felger
Michael T White
author_facet Aurel Holzschuh
Maria Gruenberg
Natalie E Hofmann
Rahel Wampfler
Benson Kiniboro
Leanne J Robinson
Ivo Mueller
Ingrid Felger
Michael T White
author_sort Aurel Holzschuh
title Co-infection of the four major Plasmodium species: Effects on densities and gametocyte carriage.
title_short Co-infection of the four major Plasmodium species: Effects on densities and gametocyte carriage.
title_full Co-infection of the four major Plasmodium species: Effects on densities and gametocyte carriage.
title_fullStr Co-infection of the four major Plasmodium species: Effects on densities and gametocyte carriage.
title_full_unstemmed Co-infection of the four major Plasmodium species: Effects on densities and gametocyte carriage.
title_sort co-infection of the four major plasmodium species: effects on densities and gametocyte carriage.
publisher Public Library of Science (PLoS)
publishDate 2022
url https://doi.org/10.1371/journal.pntd.0010760
https://doaj.org/article/cb7ba1da20224a2f805c1d15eddb6829
geographic Arctic
geographic_facet Arctic
genre Arctic
genre_facet Arctic
op_source PLoS Neglected Tropical Diseases, Vol 16, Iss 9, p e0010760 (2022)
op_relation https://doi.org/10.1371/journal.pntd.0010760
https://doaj.org/toc/1935-2727
https://doaj.org/toc/1935-2735
1935-2727
1935-2735
doi:10.1371/journal.pntd.0010760
https://doaj.org/article/cb7ba1da20224a2f805c1d15eddb6829
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container_title PLOS Neglected Tropical Diseases
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