Quantifying prevalence and risk factors of HIV multiple infection in Uganda from population-based deep-sequence data.

People living with HIV can acquire secondary infections through a process called superinfection, giving rise to simultaneous infection with genetically distinct variants (multiple infection). Multiple infection provides the necessary conditions for the generation of novel recombinant forms of HIV an...

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Main Authors: Michael A Martin, Andrea Brizzi, Xiaoyue Xi, Ronald Moses Galiwango, Sikhulile Moyo, Deogratius Ssemwanga, Alexandra Blenkinsop, Andrew D Redd, Lucie Abeler-Dörner, Christophe Fraser, Steven J Reynolds, Thomas C Quinn, Joseph Kagaayi, David Bonsall, David Serwadda, Gertrude Nakigozi, Godfrey Kigozi, M Kate Grabowski, Oliver Ratmann, with the PANGEA-HIV Consortium and the Rakai Health Sciences Program
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2025-04-01
Series:PLoS Pathogens
Online Access:https://doi.org/10.1371/journal.ppat.1013065
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author Michael A Martin
Andrea Brizzi
Xiaoyue Xi
Ronald Moses Galiwango
Sikhulile Moyo
Deogratius Ssemwanga
Alexandra Blenkinsop
Andrew D Redd
Lucie Abeler-Dörner
Christophe Fraser
Steven J Reynolds
Thomas C Quinn
Joseph Kagaayi
David Bonsall
David Serwadda
Gertrude Nakigozi
Godfrey Kigozi
M Kate Grabowski
Oliver Ratmann
with the PANGEA-HIV Consortium and the Rakai Health Sciences Program
author_facet Michael A Martin
Andrea Brizzi
Xiaoyue Xi
Ronald Moses Galiwango
Sikhulile Moyo
Deogratius Ssemwanga
Alexandra Blenkinsop
Andrew D Redd
Lucie Abeler-Dörner
Christophe Fraser
Steven J Reynolds
Thomas C Quinn
Joseph Kagaayi
David Bonsall
David Serwadda
Gertrude Nakigozi
Godfrey Kigozi
M Kate Grabowski
Oliver Ratmann
with the PANGEA-HIV Consortium and the Rakai Health Sciences Program
author_sort Michael A Martin
collection DOAJ
description People living with HIV can acquire secondary infections through a process called superinfection, giving rise to simultaneous infection with genetically distinct variants (multiple infection). Multiple infection provides the necessary conditions for the generation of novel recombinant forms of HIV and may worsen clinical outcomes and increase the rate of transmission to HIV seronegative sexual partners. To date, studies of HIV multiple infection have relied on insensitive bulk-sequencing, labor intensive single genome amplification protocols, or deep-sequencing of short genome regions. Here, we identified multiple infections in whole-genome or near whole-genome HIV RNA deep-sequence data generated from plasma samples of 2,029 people living with viremic HIV who participated in the population-based Rakai Community Cohort Study (RCCS). We estimated individual- and population-level probabilities of being multiply infected and assessed epidemiological risk factors using the novel Bayesian deep-phylogenetic multiple infection model (deep - phyloMI) which accounts for bias due to partial sequencing success and false-negative and false-positive detection rates. We estimated that between 2010 and 2020, 4.09% (95% highest posterior density interval (HPD) 2.95%-5.45%) of RCCS participants with viremic HIV multiple infection at time of sampling. Participants living in high-HIV prevalence communities along Lake Victoria were 2.33-fold (95% HPD 1.3-3.7) more likely to harbor a multiple infection compared to individuals in lower prevalence neighboring communities. This work introduces a high-throughput surveillance framework for identifying people with multiple HIV infections and quantifying population-level prevalence and risk factors of multiple infection for clinical and epidemiological investigations.
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spelling doaj-art-116c07d623ad4b2ab92d6183d624fe332025-08-20T03:25:45ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742025-04-01214e101306510.1371/journal.ppat.1013065Quantifying prevalence and risk factors of HIV multiple infection in Uganda from population-based deep-sequence data.Michael A MartinAndrea BrizziXiaoyue XiRonald Moses GaliwangoSikhulile MoyoDeogratius SsemwangaAlexandra BlenkinsopAndrew D ReddLucie Abeler-DörnerChristophe FraserSteven J ReynoldsThomas C QuinnJoseph KagaayiDavid BonsallDavid SerwaddaGertrude NakigoziGodfrey KigoziM Kate GrabowskiOliver Ratmannwith the PANGEA-HIV Consortium and the Rakai Health Sciences ProgramPeople living with HIV can acquire secondary infections through a process called superinfection, giving rise to simultaneous infection with genetically distinct variants (multiple infection). Multiple infection provides the necessary conditions for the generation of novel recombinant forms of HIV and may worsen clinical outcomes and increase the rate of transmission to HIV seronegative sexual partners. To date, studies of HIV multiple infection have relied on insensitive bulk-sequencing, labor intensive single genome amplification protocols, or deep-sequencing of short genome regions. Here, we identified multiple infections in whole-genome or near whole-genome HIV RNA deep-sequence data generated from plasma samples of 2,029 people living with viremic HIV who participated in the population-based Rakai Community Cohort Study (RCCS). We estimated individual- and population-level probabilities of being multiply infected and assessed epidemiological risk factors using the novel Bayesian deep-phylogenetic multiple infection model (deep - phyloMI) which accounts for bias due to partial sequencing success and false-negative and false-positive detection rates. We estimated that between 2010 and 2020, 4.09% (95% highest posterior density interval (HPD) 2.95%-5.45%) of RCCS participants with viremic HIV multiple infection at time of sampling. Participants living in high-HIV prevalence communities along Lake Victoria were 2.33-fold (95% HPD 1.3-3.7) more likely to harbor a multiple infection compared to individuals in lower prevalence neighboring communities. This work introduces a high-throughput surveillance framework for identifying people with multiple HIV infections and quantifying population-level prevalence and risk factors of multiple infection for clinical and epidemiological investigations.https://doi.org/10.1371/journal.ppat.1013065
spellingShingle Michael A Martin
Andrea Brizzi
Xiaoyue Xi
Ronald Moses Galiwango
Sikhulile Moyo
Deogratius Ssemwanga
Alexandra Blenkinsop
Andrew D Redd
Lucie Abeler-Dörner
Christophe Fraser
Steven J Reynolds
Thomas C Quinn
Joseph Kagaayi
David Bonsall
David Serwadda
Gertrude Nakigozi
Godfrey Kigozi
M Kate Grabowski
Oliver Ratmann
with the PANGEA-HIV Consortium and the Rakai Health Sciences Program
Quantifying prevalence and risk factors of HIV multiple infection in Uganda from population-based deep-sequence data.
PLoS Pathogens
title Quantifying prevalence and risk factors of HIV multiple infection in Uganda from population-based deep-sequence data.
title_full Quantifying prevalence and risk factors of HIV multiple infection in Uganda from population-based deep-sequence data.
title_fullStr Quantifying prevalence and risk factors of HIV multiple infection in Uganda from population-based deep-sequence data.
title_full_unstemmed Quantifying prevalence and risk factors of HIV multiple infection in Uganda from population-based deep-sequence data.
title_short Quantifying prevalence and risk factors of HIV multiple infection in Uganda from population-based deep-sequence data.
title_sort quantifying prevalence and risk factors of hiv multiple infection in uganda from population based deep sequence data
url https://doi.org/10.1371/journal.ppat.1013065
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