Male circumcision significantly reduces prevalence and load of genital anaerobic bacteria

mBio

Volumn 4, Issue 2, 2013, Pages

  Liu, Cindy M ^a,b,c   Hungate, Bruce A ^b   Tobian, Aaron A R ^c   Serwadda, David ^d   Ravel, Jacques ^e   Lester, Richard ^a   Kigozi, Godfrey ^d   Aziz, Maliha ^a   Galiwango, Ronald M ^d   Nalugoda, Fred ^d   Contente Cuomo, Tania L ^a   Wawer, Maria J ^f   Keim, Paul ^a,b   Gray, Ronald H ^f   Price, Lance B ^a,g  

^a TRANSLATIONAL GENOMICS RESEARCH INSTITUTE   (United States)

^b NORTHERN ARIZONA UNIVERSITY   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d University of Maryland School of Medicine ^*

^e UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^f JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^g GEORGE WASHINGTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RNA 16S; BACTERIAL DNA; RIBOSOME DNA;

ADOLESCENT; ADULT; ANAEROBIC BACTERIUM; ARTICLE; BACTERIAL LOAD; BAYES THEOREM; CIRCUMCISION; CONTROLLED STUDY; CORONAL SULCUS; FOLLOW UP; HUMAN; LOG RESPONSE RATIO; MALE; MICROBIAL DIVERSITY; MICROBIOME; NONHUMAN; NONMETRIC MULTIDIMENSIONAL SCALING; PENIS; PENIS MICROBIOME; PERMUTATIONAL MULTIVARIATE ANALYSIS OF VARIANCE; POLYMERASE CHAIN REACTION; PREVALENCE; PRIORITY JOURNAL; PYROSEQUENCING; RANDOMIZED CONTROLLED TRIAL; STATISTICAL ANALYSIS; TAXONOMY; UGANDA; BIODIVERSITY; CHEMISTRY; CLASSIFICATION; CONTROLLED CLINICAL TRIAL; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; MIDDLE AGED; REAL TIME POLYMERASE CHAIN REACTION;

ADOLESCENT; ADULT; BACTERIA, ANAEROBIC; BACTERIAL LOAD; BIODIVERSITY; CIRCUMCISION, MALE; DNA, BACTERIAL; DNA, RIBOSOMAL; FOLLOW-UP STUDIES; HUMANS; MALE; MIDDLE AGED; PENIS; REAL-TIME POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S; UGANDA; YOUNG ADULT;

EID: 84880072953     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00076-13     Document Type: Article

References (39)

1. Gray RH, Kigozi G, Serwadda D, Makumbi F, Watya S, Nalugoda F, Kiwanuka N, Moulton LH, Chaudhary MA, Chen MZ, Sewankambo NK, Wabwire-Mangen F, Bacon MC, Williams CF, Opendi P, Reynolds SJ, Laeyendecker O, Quinn TC, Wawer MJ. 2007. Male circumcision for HIV prevention in men in Rakai, Uganda: a randomised trial. Lancet 369:657-666.
2. Auvert B, Taljaard D, Lagarde E, Sobngwi-Tambekou J, Sitta R, Puren A. 2005. Randomized, controlled intervention trial of male circumcision for reduction of HIV infection risk: the ANRS 1265 trial. PLoS Med. 2:e298. http://dx.doi.org/10.1371/journal.pmed.0020298.
3. Bailey RC, Moses S, Parker CB, Agot K, Maclean I, Krieger JN, Williams CF, Campbell RT, Ndinya-Achola JO. 2007. Male circumcision for HIV prevention in young men in Kisumu, Kenya: a randomised controlled trial. Lancet 369:643-656.
4. Tobian AA, Serwadda D, Quinn TC, Kigozi G, Gravitt PE, Laeyendecker O, Charvat B, Ssempijja V, Riedesel M, Oliver AE, Nowak RG, Moulton LH, Chen MZ, Reynolds SJ, Wawer MJ, Gray RH. 2009. Male circumcision for the prevention of HSV-2 and HPV infections and syphilis. N. Engl. J. Med. 360:1298-1309.
5. Gray RH, Serwadda D, Kong X, Makumbi F, Kigozi G, Gravitt PE, Watya S, Nalugoda F, Ssempijja V, Tobian AA, Kiwanuka N, Moulton LH, Sewankambo NK, Reynolds SJ, Quinn TC, Iga B, Laeyendecker O, Oliver AE, Wawer MJ. 2010. Male circumcision decreases acquisition and increases clearance of high-risk human papillomavirus in HIV-negative men: a randomized trial in Rakai, Uganda. J. Infect. Dis. 201:1455-1462.
6. Gray RH, Kigozi G, Serwadda D, Makumbi F, Nalugoda F, Watya S, Moulton L, Chen MZ, Sewankambo NK, Kiwanuka N, Sempijja V, Lutalo T, Kagayii J, Wabwire-Mangen F, Ridzon R, Bacon M, Wawer MJ. 2009. The effects of male circumcision on female partners' genital tract symptoms and vaginal infections in a randomized trial in Rakai, Uganda. Am. J. Obstet. Gynecol. 2000:42.e1-42.e7. http://dx.doi.org/10.1016/j.ajog.2008.07.069.
7. Sobngwi-Tambekou J, Taljaard D, Nieuwoudt M, Lissouba P, Puren A, Auvert B. 2009. Male circumcision and Neisseria gonorrhoeae, Chlamydia trachomatis and Trichomonas vaginalis: observations after a randomised controlled trial for HIV prevention. Sex. Transm. Infect. 85:116-120.
8. Mehta SD, Moses S, Agot K, Parker C, Ndinya-Achola JO, Maclean I, Bailey RC. 2009. Adult male circumcision does not reduce the risk of incident Neisseria gonorrhoeae, Chlamydia trachomatis, or Trichomonas vaginalis infection: results from a randomized, controlled trial in Kenya. J. Infect. Dis. 200:370-378.
9. Wawer MJ, Tobian AA, Kigozi G, Kong X, Gravitt PE, Serwadda D, Nalugoda F, Makumbi F, Ssempiija V, Sewankambo N, Watya S, Eaton KP, Oliver AE, Chen MZ, Reynolds SJ, Quinn TC, Gray RH. 2011. Effect of circumcision of HIV-negative men on transmission of human papillomavirus to HIV-negative women: a randomised trial in Rakai, Uganda. Lancet 377:209-218.
10. Tobian AA, Quinn TC, Gray RH. 2011. Male circumcision for prevention of oncogenic HPV infection. Lancet 378:314-315; author reply, 315.
11. Dinh MH, Fahrbach KM, Hope TJ. 2011. The role of the foreskin in male circumcision: an evidence-based review. Am. J. Reprod. Immunol. 65: 279-283.
12. Johnson KE, Redd AD, Quinn TC, Collinson-Streng AN, Cornish T, Kong X, Sharma R, Tobian AA, Tsai B, Sherman ME, Kigozi G, Serwadda D, Wawer MJ, Gray RH. 2011. Effects of HIV-1 and herpes simplex virus type 2 infection on lymphocyte and dendritic cell density in adult foreskins from Rakai, Uganda. J. Infect. Dis. 203:602-609.
13. Glynn JR, Biraro S, Weiss HA. 2009. Herpes simplex virus type 2: a key role in HIV incidence. AIDS 23:1595-1598.
14. Celum C, Levine R, Weaver M, Wald A. 2004. Genital herpes and human immunodeficiency virus: double trouble. Bull. World Health Organ. 82: 447-453.
15. Gray RH, Wawer MJ. 2008. Reassessing the hypothesis on STI control for HIV prevention. Lancet 371:2064-2065.
16. Gray RH, Serwadda D, Tobian AA, Chen MZ, Makumbi F, Suntoke T, Kigozi G, Nalugoda F, Iga B, Quinn TC, Moulton LH, Laeyendecker O, Reynolds SJ, Kong X, Wawer MJ. 2009. Effects of genital ulcer disease and herpes simplex virus type 2 on the efficacy of male circumcision for HIV prevention: analyses from the Rakai trials. PLoS Med. 6:e1000187. http://dx.doi.org/10.1371/journal.pmed.1000187.
17. Price LB, Liu CM, Johnson KE, Aziz M, Lau MK, Bowers J, Ravel J, Keim PS, Serwadda D, Wawer MJ, Gray RH. 2010. The effects of circumcision on the penis microbiome. PLoS One 5:e8422. http://dx.doi.org/10.1371/journal.pone.0008422.
18. Flacher V, Bouschbacher M, Verronèse E, Massacrier C, Sisirak V, Berthier-Vergnes O, de Saint-Vis B, Caux C, Dezutter-Dambuyant C, Lebecque S, Valladeau J. 2006. Human Langerhans cells express a specific TLR profile and differentially respond to viruses and Gram-positive bacteria. J. Immunol. 177:7959-7967.
19. Zhang J, Li G, Bafica A, Pantelic M, Zhang P, Broxmeyer H, Liu Y, Wetzler L, He JJ, Chen T. 2005. Neisseria gonorrhoeae enhances infection of dendritic cells by HIV type 1. J. Immunol. 174:7995-8002.
20. Donoval BA, Landay AL, Moses S, Agot K, Ndinya-Achola JO, Nyagaya EA, MacLean I, Bailey RC. 2006. HIV-1 target cells in foreskins of African men with varying histories of sexually transmitted infections. Am. J. Clin. Pathol. 125:386-391.
21. Patterson BK, Landay A, Siegel JN, Flener Z, Pessis D, Chaviano A, Bailey RC. 2002. Susceptibility to human immunodeficiency virus-1 infection of human foreskin and cervical tissue grown in explant culture. Am. J. Pathol. 161:867-873.
22. Ogawa Y, Kawamura T, Kimura T, Ito M, Blauvelt A, Shimada S. 2009. Gram-positive bacteria enhance HIV-1 susceptibility in Langerhans cells, but not in dendritic cells, via Toll-like receptor activation. Blood 113: 5157-5166.
23. McGowin CL, Ma L, Martin DH, Pyles RB. 2009. Mycoplasma genitalium-encoded MG309 activates NF-kappaB via Toll-like receptors 2 and 6 to elicit proinflammatory cytokine secretion from human genital epithelial cells. Infect. Immun. 77:1175-1181.
24. de Jong MA, Geijtenbeek TB. 2009. Human immunodeficiency virus-1 acquisition in genital mucosa: Langerhans cells as key-players. J. Intern. Med. 265:18-28.
25. de Witte L, Nabatov A, Geijtenbeek TB. 2008. Distinct roles for DCSIGN +-dendritic cells and Langerhans cells in HIV-1 transmission. Trends Mol. Med. 14:12-19.
26. Eren AM, Zozaya M, Taylor CM, Dowd SE, Martin DH, Ferris MJ. 2011. Exploring the diversity of Gardnerella vaginalis in the genitourinary tract microbiota of monogamous couples through subtle nucleotide variation. PLoS One 6:e26732. http://dx.doi.org/10.1371/journal.pone.0026732.
27. Collins MD, Facklam RR, Rodrigues UM, Ruoff KL. 1993. Phylogenetic analysis of some Aerococcus-like organisms from clinical sources: description of Helcococcus kunzii gen. nov., sp. nov. Int. J. Syst. Bacteriol. 43: 425-429.
28. Liu CM, Aziz M, Kachur S, Hsueh PR, Huang YT, Keim P, Price LB. 2012. BactQuant: an enhanced broad-coverage bacterial quantitative realtime PCR assay. BMC Microbiol. 12:56. http://dx.doi.org/10.1186/1471-2180-12-56.
29. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194-2200.
30. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7:335-336.
31. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed- Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM. 2009. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 37:D141-D145. http://dx.doi.org/10.1093/nar/gkn879.
32. Lajeunessei MJ. 2011. On the meta-analysis of response ratios for studies with correlated and multi-group designs. Ecology 92:2049-2055.
33. R Development Core Team. 2011. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
34. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens HH, Wagner H. 2011. Vegan: community ecology package. R package version 1.17-8.
35. Kindt RC. 2005. Tree diversity analysis. In A manual and software for common statistical methods for ecological and biodiversity studies. World Agroforestry Centre (ICRAF), Nairobi, Kenya.
36. Goslee SC, Urban DL. 2007. The ecodist package for dissimilarity-based analysis of ecological data. J. Stat. Softw. 7:1-19.
37. Simpson EH. 1949. Measurement of diversity. Nature 163:688.
38. Roberts DW. 2010. labdsv: ordination and multivariate analysis for ecology. http://CRAN.R-project.org/package_labdsv.
39. Buchanan RE, Gibbons NE (ed). 1974. Bergey's manual of determinative bacteriology, 8th ed, vol 26. Williams & Wilkins Co., Baltimore, MD.