Male Circumcision Significantly Reduces Prevalence and Load of Genital Anaerobic Bacteria

Author:

Liu Cindy M.123,Hungate Bruce A.4,Tobian Aaron A. R.3,Serwadda David5,Ravel Jacques6,Lester Richard1,Kigozi Godfrey5,Aziz Maliha1,Galiwango Ronald M.5,Nalugoda Fred5,Contente-Cuomo Tania L.1,Wawer Maria J.7,Keim Paul12,Gray Ronald H.7,Price Lance B.18

Affiliation:

1. Division of Pathogen Genomics, Translational Genomics Research Institute, Flagstaff, Arizona, USA

2. Center for Microbial Genetics and Genomics, Northern Arizona University, Flagstaff, Arizona, USA

3. Department of Pathology, School of Medicine, Johns Hopkins University, Baltimore, Maryland, USA

4. Department of Biological Sciences, Northern Arizona University, Flagstaff, Arizona, USA

5. Rakai Health Sciences Program, Entebbe, Uganda

6. Institute for Genome Sciences, Department of Microbiology and Immunology, University of Maryland, School of Medicine, Baltimore, Maryland, USA

7. Department of Epidemiology, Johns Hopkins University, Bloomberg School of Public Health, Baltimore, Maryland, USA

8. Department of Environmental and Occupational Health, George Washington University, Washington, DC, USA

Abstract

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.

Publisher

American Society for Microbiology

Subject

Virology,Microbiology

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