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Research Article

Male Circumcision Significantly Reduces Prevalence and Load of Genital Anaerobic Bacteria

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
Andrew B. Onderdonk, Editor
Cindy M. Liu
Division of Pathogen Genomics, Translational Genomics Research Institute, Flagstaff, Arizona, USACenter for Microbial Genetics and Genomics, Northern Arizona University, Flagstaff, Arizona, USADepartment of Pathology, School of Medicine, Johns Hopkins University, Baltimore, Maryland, USA
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Bruce A. Hungate
Department of Biological Sciences, Northern Arizona University, Flagstaff, Arizona, USA
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Aaron A. R. Tobian
Department of Pathology, School of Medicine, Johns Hopkins University, Baltimore, Maryland, USA
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David Serwadda
Rakai Health Sciences Program, Entebbe, Uganda
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Jacques Ravel
Institute for Genome Sciences, Department of Microbiology and Immunology, University of Maryland, School of Medicine, Baltimore, Maryland, USA
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Richard Lester
Division of Pathogen Genomics, Translational Genomics Research Institute, Flagstaff, Arizona, USA
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Godfrey Kigozi
Rakai Health Sciences Program, Entebbe, Uganda
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Maliha Aziz
Division of Pathogen Genomics, Translational Genomics Research Institute, Flagstaff, Arizona, USA
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Ronald M. Galiwango
Rakai Health Sciences Program, Entebbe, Uganda
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Fred Nalugoda
Rakai Health Sciences Program, Entebbe, Uganda
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Tania L. Contente-Cuomo
Division of Pathogen Genomics, Translational Genomics Research Institute, Flagstaff, Arizona, USA
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Maria J. Wawer
Department of Epidemiology, Johns Hopkins University, Bloomberg School of Public Health, Baltimore, Maryland, USA
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Paul Keim
Division of Pathogen Genomics, Translational Genomics Research Institute, Flagstaff, Arizona, USACenter for Microbial Genetics and Genomics, Northern Arizona University, Flagstaff, Arizona, USA
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Ronald H. Gray
Department of Epidemiology, Johns Hopkins University, Bloomberg School of Public Health, Baltimore, Maryland, USA
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Lance B. Price
Division of Pathogen Genomics, Translational Genomics Research Institute, Flagstaff, Arizona, USADepartment of Environmental and Occupational Health, George Washington University, Washington, DC, USA
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Andrew B. Onderdonk
Brigham and Women’s Hospital
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DOI: 10.1128/mBio.00076-13
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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.

  • Copyright © 2013 Liu et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

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Male Circumcision Significantly Reduces Prevalence and Load of Genital Anaerobic Bacteria
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
mBio Apr 2013, 4 (2) e00076-13; DOI: 10.1128/mBio.00076-13

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Male Circumcision Significantly Reduces Prevalence and Load of Genital Anaerobic Bacteria
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
mBio Apr 2013, 4 (2) e00076-13; DOI: 10.1128/mBio.00076-13
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