Altered vaginal microbiota are associated with perinatal mother-to-child transmission of HIV in African women from Burkina Faso

Journal of Acquired Immune Deficiency Syndromes

Volumn 60, Issue 3, 2012, Pages 299-306

  Frank, Daniel N ^a,b   Manigart, Olivier ^c   Leroy, Valériane ^d   Meda, Nicolas ^d,e   Valéa, Diane ^f,g   Zhang, Weiming ^d   Dabis, François ^h   Pace, Norman R ^b,i   Van De Perre, Philippe ^f,g   Janoff, Edward N ^a,b,d  

^a Division of Infectious Diseases   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^c LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^d INSERM   (France)

^e UNIV MONTPELLIER   (France)

^f MONTPELLIER UNIVERSITY HOSPITAL   (France)

^g Global Health and Health Disparities   (United States)

^h UNIVERSITY OF COLORADO   (United States)

ⁱ VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

HIV AIDS; microbial ecology; microbiota; phylogenetic analysis; rRNA

Indexed keywords

BENZALKONIUM CHLORIDE; PLACEBO; RIBOSOME RNA; ZIDOVUDINE;

ARTICLE; BACTERIAL GENE; BURKINA FASO; CD4+ T LYMPHOCYTE; CLINICAL FEATURE; CLINICAL TRIAL (TOPIC); CONTROLLED STUDY; CORRELATIONAL STUDY; DOUBLE BLIND PROCEDURE; FEMALE; GARDNERELLA VAGINALIS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HUMAN TISSUE; INTRAUTERINE INFECTION; LACTOBACILLUS CASEI; LOGISTIC REGRESSION ANALYSIS; MAJOR CLINICAL STUDY; MICROBIAL COMMUNITY; MOTHER CHILD RELATION; MULTICENTER STUDY; NEWBORN; NUCLEOTIDE SEQUENCE; PERINATAL INFECTION; PRIORITY JOURNAL; PYROSEQUENCING; RANDOMIZED CONTROLLED TRIAL; RETROSPECTIVE STUDY; RISK; SEXUAL TRANSMISSION; SINGLE DRUG DOSE; VAGINA FLORA; VAGINA MUCOSA; VIRUS TRANSMISSION;

BASE SEQUENCE; BURKINA FASO; DOUBLE-BLIND METHOD; FEMALE; GENES, BACTERIAL; HIV INFECTIONS; HUMANS; INFANT, NEWBORN; INFECTIOUS DISEASE TRANSMISSION, VERTICAL; METAGENOME; MOLECULAR SEQUENCE DATA; PHYLOGENY; PREGNANCY; PREGNANCY COMPLICATIONS, INFECTIOUS; RETROSPECTIVE STUDIES; RNA, BACTERIAL; RNA, RIBOSOMAL, 16S; VAGINA;

EID: 84864298068     PISSN: 15254135     EISSN: 10779450     Source Type: Journal    
DOI: 10.1097/QAI.0b013e31824e4bdb     Document Type: Article

References (52)

1. Rollins NC, Dedicoat M, Danaviah S, et al. Prevalence, incidence, and mother-to-child transmission of HIV-1 in rural South Africa. Lancet. 2002;360:389.
2. Fowler MG, Lampe MA, Jamieson DJ, et al. Reducing the risk of mother-to-child human immunodeficiency virus transmission: past successes, current progress and challenges, and future directions. Am J Obstet Gynecol. 2007;197(3 suppl):S3-S9.
3. Dabis F, Msellati P, Meda N, et al. 6-month efficacy, tolerance, and acceptability of a short regimen of oral zidovudine to reduce vertical transmission of HIV in breastfed children in Cote d'Ivoire and Burkina Faso: a double-blind placebo-controlled multicentre trial. DITRAME Study Group. DIminution de la Transmission Mère-Enfant. Lancet. 1999;353:786-792.
4. Guay LA, Musoke P, Fleming T, et al. Intrapartum and neonatal single-dose nevirapine compared with zidovudine for prevention of mother-to-child transmission of HIV-1 in Kampala, Uganda: HIVNET 012 randomised trial. Lancet. 1999;354:795-802.
5. Chasela CS, Hudgens MG, Jamieson DJ, et al. Maternal or infant antiretroviral drugs to reduce HIV-1 transmission. N Engl J Med. 2010;362: 2271-2281.
6. Shapiro RL, Hughes MD, Ogwu A, et al. Antiretroviral regimens in pregnancy and breast-feeding in Botswana. N Engl J Med. 2010;362: 2282-2294.
7. 2006 Report on the Global AIDS Epidemic. Available at: http://data. unaids.org/pub/GlobalReport/2006/2006-GR-CH06-en.pdf. Accessed February 24, 2010.
8. Atashili J, Poole C, Ndumbe PM, et al. Bacterial vaginosis and HIV acquisition: a meta-analysis of published studies. AIDS. 2008;22:1493-1501.
9. Myer L, Denny L, Telerant R, et al. Bacterial vaginosis and susceptibility to HIV infection in South African women: a nested case-control study. J Infect Dis. 2005;192:1372-1380.
10. Taha TE, Kumwenda NI, Kafulafula G, et al. Intermittent intravaginal antibiotic treatment of bacterial vaginosis in HIV-uninfected and-infected women: a randomized clinical trial. PLoS Clin Trials. 2007;2:e10.
11. van de Wijgert JH, Morrison CS, Brown J, et al. Disentangling contributions of reproductive tract infections to HIV acquisition in African Women. Sex Transm Dis. 2009;36:357-364.
12. van de Wijgert JH, Morrison CS, Cornelisse PG, et al. Bacterial vaginosis and vaginal yeast, but not vaginal cleansing, increase HIV-1 acquisition in African women. J Acquir Immune Defic Syndr. 2008;48:203-210.
13. Farquhar C, Mbori-Ngacha D, Overbaugh J, et al. Illness during pregnancy and bacterial vaginosis are associated with in-utero HIV-1 transmission. AIDS. 2010;24:153-155.
14. Cherpes TL, Hillier SL, Meyn LA, et al. A delicate balance: risk factors for acquisition of bacterial vaginosis include sexual activity, absence of hydrogen peroxide-producing lactobacilli, black race, and positive herpes simplex virus type 2 serology. Sex Transm Dis. 2008;35:78-83.
15. Patterson JL, Stull-Lane A, Girerd PH, et al. Analysis of adherence, biofilm formation and cytotoxicity suggests a greater virulence potential of Gardnerella vaginalis relative to other bacterial-vaginosis-associated anaerobes. Microbiology. 2010;156(pt 2):392-399.
16. DiGiulio DB, Romero R, Amogan HP, et al. Microbial prevalence, diversity and abundance in amniotic fluid during preterm labor: a molecular and culture-based investigation. PLoS One. 2008;3:e3056.
17. Taha TE, Hoover DR, Dallabetta GA, et al. Bacterial vaginosis and disturbances of vaginal flora: association with increased acquisition of HIV. AIDS. 1998;12:1699-1706.
18. Group TIPH. Duration of ruptured membranes and vertical transmission of HIV-1: a meta-analysis from 15 prospective cohort studies. AIDS. 2001;15:357-368.
19. European Mode of Delivery Collaboration. Elective caesarean-section versus vaginal delivery in prevention of vertical HIV-1 transmission: a randomised clinical trial. Lancet. 1999;353:1035-1039.
20. Msellati P, Meda N, Welffens-Ekra C, et al. Zidovudine and reduction of vertical transmission of HIV in Africa. ANRS 049 Trial Group. Am J Public Health. 1999;89:947-948.
21. Msellati P, Meda N, Leroy V, et al. Safety and acceptability of vaginal disinfection with benzalkonium chloride in HIV infected pregnant women in west Africa: ANRS 049b phase II randomized, double blinded placebo controlled trial. DITRAME Study Group. Sex Transm Infect. 1999;75:420-425.
22. Mandelbrot L, Msellati P, Meda N, et al. 15 Month follow up of African children following vaginal cleansing with benzalkonium chloride of their HIV infected mothers during late pregnancy and delivery. Sex Transm Infect. 2002;78:267-270.
23. Newell ML. Mechanisms and timing of mother-to-child transmission of HIV-1. AIDS. 1998;12:831-837.
24. Frank DN, St Amand AL, Feldman RA, et al. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci USA. 2007;104: 13780-13785.
25. Frank DN, Feazel LM, Bessesen MT, et al. The human nasal microbiota and Staphylococcus aureus carriage. PLoS One. 2010;5:e10598.
26. Frank DN. BARCRAWL and BARTAB: software tools for the design and implementation of barcoded primers for highly multiplexed DNA sequencing. BMC Bioinformatics. 2009;10:362.
27. Pruesse E, Quast C, Knittel K, et al. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 2007;35:7188-7196.
28. Yarza P, Richter M, Peplies J, et al. The All-Species Living Tree project: a 16S rRNA-based phylogenetic tree of all sequenced type strains. Syst Appl Microbiol. 2008;31:241-250.
29. Wang Q, Garrity GM, Tiedje JM, et al. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 2007;73:5261-5267.
30. Good IJ. The population frequencies of species and the estimation of population parameters. Biometrika. 1953;40:237-264.
31. Chao A. Nonparametric estimation of the number of classes in a population. Scand J Stat. 1984;11:265-270.
32. Frank DN. XplorSeq: a software environment for integrated management and phylogenetic analysis of metagenomic sequence data. BMC Bioinformatics. 2008;9:420.
33. Lane DJ. 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M, eds. Nucleic Acid Techniques in Bacterial Systematics. New York, NY: Wiley; 1991:115-175.
34. Frank JA, Reich CI, Sharma S, et al. Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Appl Environ Microbiol. 2008;74:2461-2470.
35. R, Team DC. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2005.
36. Fox J. An R and S-Plus Companion to Applied Regression. Thousand Oaks, CA: Sage; 2002.
37. Latis GO, Simionato L, Ferraris G. Clinical assessment of gestational age in the newborn infant. Comparison of two methods. Early Hum Dev. 1981;5:29-37.
38. Oksanen J, Kindt R, Legendre P, et al. Vegan: community ecology package. R package version 1.15-1. 2008. Available at: http://cran.r-project.org/, http://vegan.r-forge.r-project.org. Accessed February 28, 2012.
39. Gregory R. Warnes. Includes R source code and/or documentation contributed by: Ben Bolker, Lodewijk Bonebakker, Robert Gentleman, Wolfgang Huber Andy Liaw, Thomas Lumley, Martin Maechler, Arni Magnusson, Steffen Moeller, Marc Schwartz and Bill Venables (2011). gplots: Various R programming tools for plotting data. R package version 2.10.1. Available at: http://CRAN.R-project.org/package=gplots. Accessed February 28, 2012.
40. Fredricks DN, Fiedler TL, Marrazzo JM. Molecular identification of bacteria associated with bacterial vaginosis. N Engl J Med. 2005;353:1899-1911.
41. Oakley BB, Fiedler TL, Marrazzo JM, et al. Diversity of human vaginal bacterial communities and associations with clinically defined bacterial vaginosis. Appl Environ Microbiol. 2008;74:4898-4909.
42. Ravel J, Gajer P, Abdo Z, et al. Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci USA. 2011;108(suppl 1):4680-4687.
43. Zhou X, Brown CJ, Abdo Z, et al. Differences in the composition of vaginal microbial communities found in healthy Caucasian and black women. ISME J. 2007;1:121-133.
44. Spear GT, Sikaroodi M, Zariffard MR, et al. Comparison of the diversity of the vaginal microbiota in HIV-infected and HIV-uninfected women with or without bacterial vaginosis. J Infect Dis. 2008;198:1131-1140.
45. Dumonceaux TJ, Schellenberg J, Goleski V, et al. Multiplex detection of bacteria associated with normal microbiota and with bacterial vaginosis in vaginal swabs by use of oligonucleotide-coupled fluorescent microspheres. J Clin Microbiol. 2009;47:4067-4077.
46. Anukam KC, Reid G. Organisms associated with bacterial vaginosis in Nigerian women as determined by PCR-DGGE and 16S rRNA gene sequence. Afr Health Sci. 2007;7:68-72.
47. Zhou X, Hansmann MA, Davis CC, et al. The vaginal bacterial communities of Japanese women resemble those of women in other racial groups. FEMS Immunol Med Microbiol. 2010;58:169-181.
48. Kiss H, Kogler B, Petricevic L, et al. Vaginal Lactobacillus microbiota of healthy women in the late first trimester of pregnancy. BJOG. 2007;114: 1402-1407.
49. Nagot N, Ouedraogo A, Defer MC, et al. Association between bacterial vaginosis and herpes simplex virus type-2 infection: implications for HIV acquisition studies. Sex Transm Infect. 2007;83:365-368.
50. Sha BE, Zariffard MR, Wang QJ, et al. Female genital-tract HIV load correlates inversely with Lactobacillus species but positively with bacterial vaginosis and Mycoplasma hominis. J Infect Dis. 2005;191:25-32.
51. Coleman JS, Hitti J, Bukusi EA, et al. Infectious correlates of HIV-1 shedding in the female upper and lower genital tracts. AIDS. 2007;21:755-759.
52. Burns DN, Landesman S, Muenz LR, et al. Cigarette smoking, premature rupture of membranes, and vertical transmission of HIV-1 among women with low CD4+ levels. J Acquir Immune Defic Syndr. 1994;7:718-726.