Lactobacillus-dominated cervicovaginal microbiota associated with reduced HIV/STI prevalence and genital HIV viral load in African women

被引:210
作者
Borgdorff, Hanneke [1 ,2 ]
Tsivtsivadze, Evgeni [3 ]
Verhelst, Rita [4 ]
Marzorati, Massimo [5 ]
Jurriaans, Suzanne [6 ]
Ndayisaba, Gilles F. [7 ]
Schuren, Frank H. [3 ]
van de Wijgert, Janneke H. H. M. [1 ,2 ,8 ]
机构
[1] Univ Amsterdam, Acad Med Ctr, Amsterdam Inst Global Hlth & Dev, NL-1105 AZ Amsterdam, Netherlands
[2] Univ Amsterdam, Acad Med Ctr, Dept Global Hlth, NL-1105 AZ Amsterdam, Netherlands
[3] TNO Microbiol & Syst Biol, Zeist, Netherlands
[4] Univ Ghent, Int Ctr Reprod Hlth, B-9000 Ghent, Belgium
[5] Univ Ghent, Fac Biosci Engn, Lab Microbial Ecol & Technol LabMET, B-9000 Ghent, Belgium
[6] Univ Amsterdam, Acad Med Ctr, Dept Med Microbiol, Lab Clin Virol, NL-1105 AZ Amsterdam, Netherlands
[7] Rinda Ubuzima, Kigali, Rwanda
[8] Univ Liverpool, Inst Infect & Global Hlth, Dept Clin Infect Microbiol & Immunol, Liverpool L69 7BE, Merseyside, England
关键词
bacterial vaginosis; cervicovaginal HIV-1 RNA; cervicovaginal microbiome; HIV; sexually transmitted infections; Rwanda; IMMUNODEFICIENCY-VIRUS TYPE-1; BACTERIAL VAGINOSIS; VAGINAL MICROBIOTA; NEISSERIA-GONORRHOEAE; INERS; IDENTIFICATION; TRANSMISSION; EXPRESSION; DIVERSITY; CRISPATUS;
D O I
10.1038/ismej.2014.26
中图分类号
Q14 [生态学(生物生态学)];
学科分类号
071012 ; 0713 ;
摘要
Cervicovaginal microbiota not dominated by lactobacilli may facilitate transmission of HIV and other sexually transmitted infections (STIs), as well as miscarriages, preterm births and sepsis in pregnant women. However, little is known about the exact nature of the microbiological changes that cause these adverse outcomes. In this study, cervical samples of 174 Rwandan female sex workers were analyzed cross-sectionally using a phylogenetic microarray. Furthermore, HIV-1 RNA concentrations were measured in cervicovaginal lavages of 58 HIV-positive women among them. We identified six microbiome clusters, representing a gradient from low semi-quantitative abundance and diversity dominated by Lactobacillus crispatus (cluster R-I, with R denoting 'Rwanda') and L. iners (R-II) to intermediate (R-V) and high abundance and diversity (R-III, R-IV and R-VI) dominated by a mixture of anaerobes, including Gardnerella, Atopobium and Prevotella species. Women in cluster R-I were less likely to have HIV (P=0.03), herpes simplex virus type 2 (HSV-2; P<0.01), and high-risk human papillomavirus (HPV; P<0.01) and had no bacterial STIs (P=0.15). Statistically significant trends in prevalence of viral STIs were found from low prevalence in cluster R-I, to higher prevalence in clusters R-II and R-V, and highest prevalence in clusters R-III/R-IV/R-VI. Furthermore, only 10% of HIV-positive women in clusters R-I/R-II, compared with 40% in cluster R-V, and 42% in clusters R-III/R-IV/R-VI had detectable cervicovaginal HIV-1 RNA (P-trend=0.03). We conclude that L. crispatus-dominated, and to a lesser extent L. iners-dominated, cervicovaginal microbiota are associated with a lower prevalence of HIV/STIs and a lower likelihood of genital HIV-1 RNA shedding.
引用
收藏
页码:1781 / 1793
页数:13
相关论文
共 62 条
[1]   Suppression of human immunodeficiency virus type 1 replication in macrophages by commensal bacteria preferentially stimulating Toll-like receptor 4 [J].
Ahmed, Nursarat ;
Hayashi, Takaya ;
Hasegawa, Atsuhiko ;
Furukawa, Hiroyuki ;
Okamura, Noboru ;
Chida, Toshio ;
Masuda, Takao ;
Kannagi, Mari .
JOURNAL OF GENERAL VIROLOGY, 2010, 91 :2804-2813
[2]   Vaginal concentrations of lactic acid potently inactivate HIV [J].
Aldunate, Muriel ;
Tyssen, David ;
Johnson, Adam ;
Zakir, Tasnim ;
Sonza, Secondo ;
Moench, Thomas ;
Cone, Richard ;
Tachedjian, Gilda .
JOURNAL OF ANTIMICROBIAL CHEMOTHERAPY, 2013, 68 (09) :2015-2025
[3]   NONSPECIFIC VAGINITIS - DIAGNOSTIC-CRITERIA AND MICROBIAL AND EPIDEMIOLOGIC ASSOCIATIONS [J].
AMSEL, R ;
TOTTEN, PA ;
SPIEGEL, CA ;
CHEN, KCS ;
ESCHENBACH, D ;
HOLMES, KK .
AMERICAN JOURNAL OF MEDICINE, 1983, 74 (01) :14-22
[4]   High Human Immunodeficiency Virus Incidence in a Cohort of Rwandan Female Sex Workers [J].
Braunstein, Sarah L. ;
Ingabire, Chantal M. ;
Kestelyn, Evelyne ;
Uwizera, Aline Umutoni ;
Mwamarangwe, Lambert ;
Ntirushwa, Justin ;
Nash, Denis ;
Veldhuijzen, Nienke J. ;
Nel, Annalene ;
Vyankandondera, Joseph ;
van de Wijgert, Janneke H. H. M. .
SEXUALLY TRANSMITTED DISEASES, 2011, 38 (05) :385-394
[5]   Reciprocal Interference between Lactobacillus spp. and Gardnerella vaginalis on Initial Adherence to Epithelial Cells [J].
Castro, Joana ;
Henriques, Ana ;
Machado, Antonio ;
Henriques, Mariana ;
Jefferson, Kimberly K. ;
Cerca, Nuno .
INTERNATIONAL JOURNAL OF MEDICAL SCIENCES, 2013, 10 (09) :1193-1198
[6]   Association between acquisition of herpes simplex virus type 2 in women and bacterial vaginosis [J].
Cherpes, TL ;
Meyn, LA ;
Krohn, MA ;
Lurie, JG ;
Hillier, SL .
CLINICAL INFECTIOUS DISEASES, 2003, 37 (03) :319-325
[7]   A WILCOXON-TYPE TEST FOR TREND [J].
CUZICK, J .
STATISTICS IN MEDICINE, 1985, 4 (01) :87-90
[8]   PCR-based identification of eight lactobacillus species and 18 hr-HPV genotypes in fixed cervical samples of south african women at risk of HIV and BV [J].
Dols, Joke A. M. ;
Reid, Gregor ;
Kort, Remco ;
Schuren, Frank H. J. ;
Tempelman, Hugo ;
Bontekoe, Tj Romke ;
Korporaal, Hans ;
Van der Veer, E. M. ;
Smit, Pieter W. ;
Boon, Mathilde E. .
DIAGNOSTIC CYTOPATHOLOGY, 2012, 40 (06) :472-477
[9]   Microarray-based identification of clinically relevant vaginal bacteria in relation to bacterial vaginosis [J].
Dols, Joke A. M. ;
Smit, Pieter W. ;
Kort, Remco ;
Reid, Gregor ;
Schuren, Frank H. J. ;
Tempelman, Hugo ;
Bontekoe, Tj. Romke ;
Korporaal, Hans ;
Boon, Mathilde E. .
AMERICAN JOURNAL OF OBSTETRICS AND GYNECOLOGY, 2011, 204 (04) :305.e1-305.e7
[10]   Characterization of the Vaginal Micro- and Mycobiome in Asymptomatic Reproductive-Age Estonian Women [J].
Drell, Tiina ;
Lillsaar, Triin ;
Tummeleht, Lea ;
Simm, Jaak ;
Aaspollu, Anu ;
Vaein, Edda ;
Saarma, Ivo ;
Salumets, Andres ;
Donders, Gilbert G. G. ;
Metsis, Madis .
PLOS ONE, 2013, 8 (01)