Male Circumcision Significantly Reduces Prevalence and Load of Genital Anaerobic Bacteria

ABSTRACT Male circumcision reduces female-to-male HIV transmission. Hypothesized mechanisms for this protective effect include decreased HIV target cell recruitment and activation due to changes in the penis microbiome. We compared the coronal sulcus microbiota of men from a group of uncircumcised c...

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Autores principales: Cindy M. Liu, Bruce A. Hungate, Aaron A. R. Tobian, David Serwadda, Jacques Ravel, Richard Lester, Godfrey Kigozi, Maliha Aziz, Ronald M. Galiwango, Fred Nalugoda, Tania L. Contente-Cuomo, Maria J. Wawer, Paul Keim, Ronald H. Gray, Lance B. Price
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Publicado: American Society for Microbiology 2013
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spelling oai:doaj.org-article:efa0f2052dd74e19b5758284919d68882021-11-15T15:40:29ZMale Circumcision Significantly Reduces Prevalence and Load of Genital Anaerobic Bacteria10.1128/mBio.00076-132150-7511https://doaj.org/article/efa0f2052dd74e19b5758284919d68882013-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00076-13https://doaj.org/toc/2150-7511ABSTRACT Male circumcision reduces female-to-male HIV transmission. Hypothesized mechanisms for this protective effect include decreased HIV target cell recruitment and activation due to changes in the penis microbiome. We compared the coronal sulcus microbiota of men from a group of uncircumcised controls (n = 77) and from a circumcised intervention group (n = 79) at enrollment and year 1 follow-up in a randomized circumcision trial in Rakai, Uganda. We characterized microbiota using16S rRNA gene-based quantitative PCR (qPCR) and pyrosequencing, log response ratio (LRR), Bayesian classification, nonmetric multidimensional scaling (nMDS), and permutational multivariate analysis of variance (PerMANOVA). At baseline, men in both study arms had comparable coronal sulcus microbiota; however, by year 1, circumcision decreased the total bacterial load and reduced microbiota biodiversity. Specifically, the prevalence and absolute abundance of 12 anaerobic bacterial taxa decreased significantly in the circumcised men. While aerobic bacterial taxa also increased postcircumcision, these gains were minor. The reduction in anaerobes may partly account for the effects of circumcision on reduced HIV acquisition. IMPORTANCE The bacterial changes identified in this study may play an important role in the HIV risk reduction conferred by male circumcision. Decreasing the load of specific anaerobes could reduce HIV target cell recruitment to the foreskin. Understanding the mechanisms that underlie the benefits of male circumcision could help to identify new intervention strategies for decreasing HIV transmission, applicable to populations with high HIV prevalence where male circumcision is culturally less acceptable.Cindy M. LiuBruce A. HungateAaron A. R. TobianDavid SerwaddaJacques RavelRichard LesterGodfrey KigoziMaliha AzizRonald M. GaliwangoFred NalugodaTania L. Contente-CuomoMaria J. WawerPaul KeimRonald H. GrayLance B. PriceAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 4, Iss 2 (2013)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
Cindy M. Liu
Bruce A. Hungate
Aaron A. R. Tobian
David Serwadda
Jacques Ravel
Richard Lester
Godfrey Kigozi
Maliha Aziz
Ronald M. Galiwango
Fred Nalugoda
Tania L. Contente-Cuomo
Maria J. Wawer
Paul Keim
Ronald H. Gray
Lance B. Price
Male Circumcision Significantly Reduces Prevalence and Load of Genital Anaerobic Bacteria
description ABSTRACT Male circumcision reduces female-to-male HIV transmission. Hypothesized mechanisms for this protective effect include decreased HIV target cell recruitment and activation due to changes in the penis microbiome. We compared the coronal sulcus microbiota of men from a group of uncircumcised controls (n = 77) and from a circumcised intervention group (n = 79) at enrollment and year 1 follow-up in a randomized circumcision trial in Rakai, Uganda. We characterized microbiota using16S rRNA gene-based quantitative PCR (qPCR) and pyrosequencing, log response ratio (LRR), Bayesian classification, nonmetric multidimensional scaling (nMDS), and permutational multivariate analysis of variance (PerMANOVA). At baseline, men in both study arms had comparable coronal sulcus microbiota; however, by year 1, circumcision decreased the total bacterial load and reduced microbiota biodiversity. Specifically, the prevalence and absolute abundance of 12 anaerobic bacterial taxa decreased significantly in the circumcised men. While aerobic bacterial taxa also increased postcircumcision, these gains were minor. The reduction in anaerobes may partly account for the effects of circumcision on reduced HIV acquisition. IMPORTANCE The bacterial changes identified in this study may play an important role in the HIV risk reduction conferred by male circumcision. Decreasing the load of specific anaerobes could reduce HIV target cell recruitment to the foreskin. Understanding the mechanisms that underlie the benefits of male circumcision could help to identify new intervention strategies for decreasing HIV transmission, applicable to populations with high HIV prevalence where male circumcision is culturally less acceptable.
format article
author Cindy M. Liu
Bruce A. Hungate
Aaron A. R. Tobian
David Serwadda
Jacques Ravel
Richard Lester
Godfrey Kigozi
Maliha Aziz
Ronald M. Galiwango
Fred Nalugoda
Tania L. Contente-Cuomo
Maria J. Wawer
Paul Keim
Ronald H. Gray
Lance B. Price
author_facet Cindy M. Liu
Bruce A. Hungate
Aaron A. R. Tobian
David Serwadda
Jacques Ravel
Richard Lester
Godfrey Kigozi
Maliha Aziz
Ronald M. Galiwango
Fred Nalugoda
Tania L. Contente-Cuomo
Maria J. Wawer
Paul Keim
Ronald H. Gray
Lance B. Price
author_sort Cindy M. Liu
title Male Circumcision Significantly Reduces Prevalence and Load of Genital Anaerobic Bacteria
title_short Male Circumcision Significantly Reduces Prevalence and Load of Genital Anaerobic Bacteria
title_full Male Circumcision Significantly Reduces Prevalence and Load of Genital Anaerobic Bacteria
title_fullStr Male Circumcision Significantly Reduces Prevalence and Load of Genital Anaerobic Bacteria
title_full_unstemmed Male Circumcision Significantly Reduces Prevalence and Load of Genital Anaerobic Bacteria
title_sort male circumcision significantly reduces prevalence and load of genital anaerobic bacteria
publisher American Society for Microbiology
publishDate 2013
url https://doaj.org/article/efa0f2052dd74e19b5758284919d6888
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