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Research Article

Penile Microbiota and Female Partner Bacterial Vaginosis in Rakai, Uganda

Cindy M. Liu, Bruce A. Hungate, Aaron A. R. Tobian, Jacques Ravel, Jessica L. Prodger, David Serwadda, Godfrey Kigozi, Ronald M. Galiwango, Fred Nalugoda, Paul Keim, Maria J. Wawer, Lance B. Price, Ronald H. Gray
Melinda M. Pettigrew, Editor
Cindy M. Liu
aDepartment of Pathology, School of Medicine, Johns Hopkins University, Baltimore, Maryland, USA
bCenter for Microbial Genetics and Genomics, Northern Arizona University, Flagstaff, Arizona, USA
cDivision of Pathogen Genomics, Translational Genomics Research Institute, Flagstaff, Arizona, USA
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Bruce A. Hungate
dCenter for Ecosystem Science and Society and Department of Biological Sciences, Northern Arizona University, Flagstaff, Arizona, USA
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Aaron A. R. Tobian
aDepartment of Pathology, School of Medicine, Johns Hopkins University, Baltimore, Maryland, USA
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Jacques Ravel
eInstitute for Genome Sciences, University of Maryland School of Medicine, Baltimore, Maryland, USA
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Jessica L. Prodger
fDepartment of Medicine, University of Toronto, Toronto, Canada
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David Serwadda
gRakai Health Sciences Program, Entebbe, Uganda
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Godfrey Kigozi
gRakai Health Sciences Program, Entebbe, Uganda
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Ronald M. Galiwango
gRakai Health Sciences Program, Entebbe, Uganda
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Fred Nalugoda
gRakai Health Sciences Program, Entebbe, Uganda
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Paul Keim
bCenter for Microbial Genetics and Genomics, Northern Arizona University, Flagstaff, Arizona, USA
cDivision of Pathogen Genomics, Translational Genomics Research Institute, Flagstaff, Arizona, USA
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Maria J. Wawer
hDepartment of Epidemiology, Johns Hopkins University, Bloomberg School of Public Health, Baltimore, Maryland, USA
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Lance B. Price
cDivision of Pathogen Genomics, Translational Genomics Research Institute, Flagstaff, Arizona, USA
iDepartment of Environmental and Occupational Health, Milken Institute School of Public Health, George Washington University, Washington, DC, USA
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Ronald H. Gray
hDepartment of Epidemiology, Johns Hopkins University, Bloomberg School of Public Health, Baltimore, Maryland, USA
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Melinda M. Pettigrew
Yale University
Roles: Editor
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DOI: 10.1128/mBio.00589-15
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ABSTRACT

Bacterial vaginosis (BV) is a common vaginal bacterial imbalance associated with risk for HIV and poor gynecologic and obstetric outcomes. Male circumcision reduces BV-associated bacteria on the penis and decreases BV in female partners, but the link between penile microbiota and female partner BV is not well understood. We tested the hypothesis that having a female partner with BV increases BV-associated bacteria in uncircumcised men. We characterized penile microbiota composition and density (i.e., the quantity of bacteria per swab) by broad-coverage 16S rRNA gene-based sequencing and quantitative PCR (qPCR) in 165 uncircumcised men from Rakai, Uganda. Associations between penile community state types (CSTs) and female partner's Nugent score were assessed. We found seven distinct penile CSTs of increasing density (CST1 to 7). CST1 to 3 and CST4 to 7 were the two major CST groups. CST4 to 7 had higher prevalence and abundance of BV-associated bacteria, such as Mobiluncus and Dialister, than CST1 to 3. Men with CST4 to 7 were significantly more likely to have a female partner with a high Nugent score (P = 0.03). Men with two or more extramarital partners were significantly more likely to have CST4 to 7 than men with only marital partners (CST4 to 7 prevalence ratio, 1.84; 95% confidence interval [CI], 1.16 to 2.92). Female partner Nugent BV is significantly associated with penile microbiota. Our data support the exchange of BV-associated bacteria through intercourse, which may explain BV recurrence and persistence.

IMPORTANCE Bacterial vaginosis (BV) is sexually associated but not considered a sexually transmitted disease. Our findings suggest that the uncircumcised penis is an important niche for BV-associated genital anaerobes. In addition, we found a link between extramarital sexual relationships and BV-associated bacteria in men, which parallels earlier findings of the association between sexual activity and BV in women. This suggests the sexual transmissibility of BV-associated bacteria. Reducing bacterial exchange by barrier methods and managing carriage of BV-associated bacteria in men may decrease BV persistence and recurrence in women.

  • Copyright © 2015 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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Penile Microbiota and Female Partner Bacterial Vaginosis in Rakai, Uganda
Cindy M. Liu, Bruce A. Hungate, Aaron A. R. Tobian, Jacques Ravel, Jessica L. Prodger, David Serwadda, Godfrey Kigozi, Ronald M. Galiwango, Fred Nalugoda, Paul Keim, Maria J. Wawer, Lance B. Price, Ronald H. Gray
mBio Jun 2015, 6 (3) e00589-15; DOI: 10.1128/mBio.00589-15

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Penile Microbiota and Female Partner Bacterial Vaginosis in Rakai, Uganda
Cindy M. Liu, Bruce A. Hungate, Aaron A. R. Tobian, Jacques Ravel, Jessica L. Prodger, David Serwadda, Godfrey Kigozi, Ronald M. Galiwango, Fred Nalugoda, Paul Keim, Maria J. Wawer, Lance B. Price, Ronald H. Gray
mBio Jun 2015, 6 (3) e00589-15; DOI: 10.1128/mBio.00589-15
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