期刊论文详细信息
BMC Infectious Diseases
The significance of Lactobacillus crispatus and L. vaginalis for vaginal health and the negative effect of recent sex: a cross-sectional descriptive study across groups of African women
Tania Crucitti4  Liselotte Hardy4  Joris Menten7  Kishor Mandaliya6  Gilles F Ndayisaba9  Mary Mwaura6  Sinead Delany-Moretlwe3  Hans Verstraelen2  Rita Verhelst5  Piet Cools1  Janneke van de Wijgert8  Vicky Jespers1,10 
[1] Laboratory Bacteriology Research, University Gent, Ghent, Belgium;Department of Obstetrics and Gynaecology, Faculty of Medicine and Health Sciences, Ghent University, Ghent, Belgium;Wits Reproductive Health & HIV Institute, University of Witwatersrand, Johannesburg, South Africa;Department of Clinical Sciences, HIV/STI Reference Laboratory, Institute of Tropical Medicine, Antwerp, Belgium;International Center for Reproductive Health (ICRH), Ghent University, Ghent, Belgium;ICRH Kenya, Mombasa, Kenya;Department of Clinical Sciences, Institute of Tropical Medicine, Antwerp, Belgium;Department of Clinical Infection, Microbiology and Immunology, Institute of Infection and Global Health, University of Liverpool, Liverpool, UK;Rinda Ubuzima, Kigali, Rwanda;Department of Public Health, Unit of Epidemiology and Control of HIV/STD, Institute of Tropical Medicine, Nationalestraat 155, Antwerp, B-2000, Belgium
关键词: HIV prevention;    Sexual health;    Vaginal microbiota;    Sub-Saharan Africa;    quantitative PCR;    Sexually transmitted infections;    Lactobacillus, reproductive health;    Bacterial vaginosis;   
Others  :  1135421
DOI  :  10.1186/s12879-015-0825-z
 received in 2014-09-12, accepted in 2015-02-10,  发布年份 2015
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【 摘 要 】

Background

Women in sub-Saharan Africa are vulnerable to acquiring HIV infection and reproductive tract infections. Bacterial vaginosis (BV), a disruption of the vaginal microbiota, has been shown to be strongly associated with HIV infection. Risk factors related to potentially protective or harmful microbiota species are not known.

Methods

We present cross-sectional quantitative polymerase chain reaction data of the Lactobacillus genus, five Lactobacillus species, and three BV-related bacteria (Gardnerella vaginalis, Atopobium vaginae, and Prevotella bivia) together with Escherichia coli and Candida albicans in 426 African women across different groups at risk for HIV. We selected a reference group of adult HIV-negative women at average risk for HIV acquisition and compared species variations in subgroups of adolescents, HIV-negative pregnant women, women engaging in traditional vaginal practices, sex workers and a group of HIV-positive women on combination antiretroviral therapy. We explored the associations between presence and quantity of the bacteria with BV by Nugent score, in relation to several factors of known or theoretical importance.

Results

The presence of species across Kenyan, South African and Rwandan women was remarkably similar and few differences were seen between the two groups of reference women in Kenya and South Africa. The Rwandan sex workers and HIV-positive women had the highest G. vaginalis presence (p = 0.006). Pregnant women had a higher Lactobacillus genus mean log (7.01 genome equivalents (geq)/ml) compared to the reference women (6.08 geq/ml). L. vaginalis (43%) was second to L. iners (81.9%) highly present in women with a normal Nugent score. Recent sexual exposure negatively affected the presence of L. crispatus (<0.001), L. vaginalis (p = 0.001), and Lactobacillus genus (p < 0.001). Having more than one sexual partner in the last three months was associated with an increased prevalence of G. vaginalis (p = 0.044) and L. iners (p = 0.001).

Conclusions

Although the composition of species across the studied African countries was similar, the presence of protective species i.e. L. crispatus and L. vaginalis in women with a normal Nugent score appeared lower compared to non-African studies. Furthermore, Lactobacillus species were negatively affected by sexual behavioural. Strategies to support protective Lactobacillus species are urgently needed.

Trial registration

The study is registered at the Trial Registration at the National Health Research Ethics Council South Africa with the number DOH2709103223.

【 授权许可】

   
2015 Jespers et al.; licensee BioMed Central.

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【 参考文献 】
  • [1]Atashili J, Poole C, Ndumbe PM, Adimora AA, Smith JS: Bacterial vaginosis and HIV acquisition: a meta-analysis of published studies. AIDS 2008, 22:1493-501.
  • [2]Taylor BD, Darville T, Haggerty CL: Does bacterial vaginosis cause pelvic inflammatory disease? Sex Transm Dis 2013, 40:117-22.
  • [3]Li J, McCormick J, Bocking A, Reid G: Importance of vaginal microbes in reproductive health. Reprod Sci 2012, 19:235-42.
  • [4]Frank DN, Manigart O, Leroy V, Meda N, Valea D, Zhang W, et al.: Altered vaginal microbiota are associated with perinatal mother-to-child transmission of HIV in African women from Burkina Faso. J Acquir Immune Defic Syndr 2012, 60:299-306.
  • [5]Cherpes TL, Meyn LA, Krohn MA, Lurie JG, Hillier SL: Association between acquisition of herpes simplex virus type 2 in women and bacterial vaginosis. Clin Infect Dis 2003, 37:319-25.
  • [6]King CC, Jamieson DJ, Wiener J, Cu-Uvin S, Klein RS, Rompalo AM, et al.: Bacterial vaginosis and the natural history of human papillomavirus. Infect Dis Obstet Gynecol 2011, 2011:319460.
  • [7]Wiesenfeld HC, Hillier SL, Krohn MA, Landers DV, Sweet RL: Bacterial vaginosis is a strong predictor of Neisseria gonorrhoeae and Chlamydia trachomatis infection. Clin Infect Dis 2003, 36:663-8.
  • [8]Buve A, Jespers V, Crucitti T, Fichorova RN: The vaginal microbiota and susceptibility to HIV. AIDS 2014, 24:2333-44.
  • [9]Srinivasan S, Fredricks DN: The human vaginal bacterial biota and bacterial vaginosis. Interdiscip Perspect Infect Dis 2008, 2008:750479.
  • [10]van de Wijgert JH, Borgdorff H, Verhelst R, Crucitti T, Francis S, Verstraelen H, et al.: The vaginal microbiota: what have we learned after a decade of molecular characterization? PLoS One 2014, 9:e105998.
  • [11]Mitchell C, Marrazzo J: Bacterial vaginosis and the cervicovaginal immune response. Am J Reprod Immunol 2014, 71:555-63.
  • [12]Hickey RJ, Zhou X, Pierson JD, Ravel J, Forney LJ: Understanding vaginal microbiome complexity from an ecological perspective. Transl Res 2012, 160:267-82.
  • [13]Jespers V, Menten J, Smet H, Poradosu S, Abdellati S, Verhelst R, et al.: Quantification of bacterial species of the vaginal microbiome in different groups of women, using nucleic acid amplification tests. BMC Microbiol 2012, 12:83. BioMed Central Full Text
  • [14]Mauck CK: Biomarkers of semen exposure. Sex Transm Dis 2009, 36:S81-3.
  • [15]Jespers V, Crucitti T, Menten J, Verhelst R, Mwaura M, Mandaliya K, et al.: Prevalence and correlates of bacterial vaginosis in different sub-populations of women in sub-Saharan Africa: a cross-sectional study. PLoS One 2014, 9:e109670.
  • [16]Braunstein SL, Ingabire CM, Kestelyn E, Uwizera AU, Mwamarangwe L, Ntirushwa J, et al.: High human immunodeficiency virus incidence in a cohort of Rwandan female sex workers. Sex Transm Dis 2011, 38:385-94.
  • [17]Braunstein SL, Ingabire CM, Geubbels E, Vyankandondera J, Umulisa MM, Gahiro E, et al.: High burden of prevalent and recently acquired HIV among female sex workers and female HIV voluntary testing center clients in Kigali, Rwanda. PLoS One 2011, 6:e24321.
  • [18]Nugent RP, Krohn MA, Hillier SL: Reliability of diagnosing bacterial vaginosis is improved by a standardized method of gram stain interpretation. J Clin Microbiol 1991, 29:297-301.
  • [19]dos Lopes Santos Santiago G, Tency I, Verstraelen H, Verhelst R, Trog M, Temmerman M, et al.: Longitudinal qPCR study of the dynamics of L. crispatus, L. iners, A. vaginae, (sialidase positive) G. vaginalis, and P. bivia in the vagina. PLoS One 2012, 7:e45281.
  • [20]Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SS, McCulle SL, et al.: Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci U S A 2011, 108(Suppl 1):4680-7.
  • [21]Tamrakar R, Yamada T, Furuta I, Cho K, Morikawa M, Yamada H, et al.: Association between Lactobacillus species and bacterial vaginosis-related bacteria, and bacterial vaginosis scores in pregnant Japanese women. BMC Infect Dis 2007, 7:128. BioMed Central Full Text
  • [22]Zariffard MR, Saifuddin M, Sha BE, Spear GT: Detection of bacterial vaginosis-related organisms by real-time PCR for Lactobacilli, Gardnerella vaginalis and Mycoplasma hominis. FEMS Immunol Med Microbiol 2002, 34:277-81.
  • [23]Mauck CK, Lai JJ, Weiner DH, Chandra N, Fichorova RN, Dezzutti CS, et al.: Toward early safety alert endpoints: exploring biomarkers suggestive of microbicide failure. AIDS Res Hum Retroviruses 2013, 29:1475-86.
  • [24]Byun R, Nadkarni MA, Chhour KL, Martin FE, Jacques NA, Hunter N: Quantitative analysis of diverse Lactobacillus species present in advanced dental caries. J Clin Microbiol 2004, 42:3128-36.
  • [25]De Backer E, Verhelst R, Verstraelen H, Alqumber MA, Burton JP, Tagg JR, et al.: Quantitative determination by real-time PCR of four vaginal Lactobacillus species, Gardnerella vaginalis and Atopobium vaginae indicates an inverse relationship between L. gasseri and L. iners. BMC Microbiol 2007, 7:115. BioMed Central Full Text
  • [26]Chern EC, Siefring S, Paar J, Doolittle M, Haugland RA: Comparison of quantitative PCR assays for Escherichia coli targeting ribosomal RNA and single copy genes. Lett Appl Microbiol 2011, 52:298-306.
  • [27]Menard JP, Fenollar F, Raoult D, Boubli L, Bretelle F: Self-collected vaginal swabs for the quantitative real-time polymerase chain reaction assay of Atopobium vaginae and Gardnerella vaginalis and the diagnosis of bacterial vaginosis. Eur J Clin Microbiol Infect Dis 2011, 31:513-8.
  • [28]Hickey RJ, Abdo Z, Zhou X, Nemeth K, Hansmann M, Osborn TW III, et al.: Effects of tampons and menses on the composition and diversity of vaginal microbial communities over time. BJOG 2013, 120:695-704.
  • [29]Jin L, Tao L, Pavlova SI, So JS, Kiwanuka N, Namukwaya Z, et al.: Species diversity and relative abundance of vaginal lactic acid bacteria from women in Uganda and Korea. J Appl Microbiol 2007, 102:1107-15.
  • [30]Gustafsson RJ, Ahrne S, Jeppsson B, Benoni C, Olsson C, Stjernquist M, et al.: The Lactobacillus flora in vagina and rectum of fertile and postmenopausal healthy Swedish women. BMC Womens Health 2011, 11:17. BioMed Central Full Text
  • [31]Mendes-Soares H, Suzuki H, Hickey RJ, Forney LJ: Comparative functional genomics of Lactobacillus spp. reveals possible mechanisms for specialization of vaginal lactobacilli to their environment. J Bacteriol 2014, 196:1458-70.
  • [32]Boskey ER, Telsch KM, Whaley KJ, Moench TR, Cone RA: Acid production by vaginal flora in vitro is consistent with the rate and extent of vaginal acidification. Infect Immun 1999, 67:5170-5.
  • [33]Anukam KC, Osazuwa EO, Ahonkhai I, Reid G: Lactobacillus vaginal microbiota of women attending a reproductive health care service in Benin city, Nigeria. Sex Transm Dis 2006, 33:59-62.
  • [34]Mitchell C, Balkus JE, Fredricks D, Liu C, McKernan-Mullin J, Frenkel LM, et al.: Interaction between lactobacilli, bacterial vaginosis-associated bacteria, and HIV Type 1 RNA and DNA Genital shedding in U.S. and Kenyan women. AIDS Res Hum Retroviruses 2013, 29:13-9.
  • [35]Benning L, Golub ET, Anastos K, French AL, Cohen M, Gilbert D, et al.: Comparison of lower genital tract microbiota in HIV-infected and uninfected women from Rwanda and the US. PLoS One 2014, 9:e96844.
  • [36]Aagaard K, Riehle K, Ma J, Segata N, Mistretta TA, Coarfa C, et al.: metagenomic approach to characterization of the vaginal microbiome signature in pregnancy. PLoS One 2012, 7:e36466.
  • [37]Petricevic L, Domig KJ, Nierscher FJ, Krondorfer I, Janitschek C, Kneifel W, et al.: Characterisation of the oral, vaginal and rectal Lactobacillus flora in healthy pregnant and postmenopausal women. Eur J Obstet Gynecol Reprod Biol 2012, 160:93-9.
  • [38]Romero R, Hassan SS, Gajer P, Tarca AL, Fadrosh DW, Nikita L, et al.: The composition and stability of the vaginal microbiota of normal pregnant women is different from that of non-pregnant women. Microbiome 2014, 2:4. BioMed Central Full Text
  • [39]Walther-Antonio MR, Jeraldo P, Berg Miller ME, Yeoman CJ, Nelson KE, Wilson BA, et al.: Pregnancy’s stronghold on the vaginal microbiome. PLoS One 2014, 9:e98514.
  • [40]Castro J, Henriques A, Machado A, Henriques M, Jefferson KK, Cerca N: Reciprocal interference between Lactobacillus spp. and Gardnerella vaginalis on initial adherence to epithelial cells. Int J Med Sci 2013, 10:1193-8.
  • [41]Zhou X, Brown CJ, Abdo Z, Davis CC, Hansmann MA, Joyce P, et al.: Differences in the composition of vaginal microbial communities found in healthy Caucasian and black women. ISME J 2007, 1:121-33.
  • [42]Zhou X, Hansmann MA, Davis CC, Suzuki H, Brown CJ, Schutte U, et al.: The vaginal bacterial communities of Japanese women resemble those of women in other racial groups. FEMS Immunol Med Microbiol 2010, 58:169-81.
  • [43]Ling Z, Kong J, Liu F, Zhu H, Chen X, Wang Y, et al.: Molecular analysis of the diversity of vaginal microbiota associated with bacterial vaginosis. BMC Genomics 2010, 11:488. BioMed Central Full Text
  • [44]Drell T, Lillsaar T, Tummeleht L, Simm J, Aaspollu A, Vain E, et al.: Characterization of the vaginal micro- and mycobiome in asymptomatic reproductive-age Estonian women. PLoS One 2013, 8:e54379.
  • [45]Shipitsyna E, Roos A, Datcu R, Hallen A, Fredlund H, Jensen JS, et al.: Composition of the vaginal microbiota in women of reproductive age–sensitive and specific molecular diagnosis of bacterial vaginosis is possible? PLoS One 2013, 8:e60670.
  • [46]Ma L, Lv Z, Su J, Wang J, Yan D, Wei J, et al.: Consistent condom use increases the colonization of Lactobacillus crispatus in the vagina. PLoS One 2013, 8:e70716.
  • [47]Marrazzo JM: Interpreting the epidemiology and natural history of bacterial vaginosis: are we still confused? Anaerobe 2011, 17:186-90.
  • [48]Schwebke JR, Desmond R: Risk factors for bacterial vaginosis in women at high risk for sexually transmitted diseases. Sex Transm Dis 2005, 32:654-8.
  • [49]Paramel Jayaprakash T, Schellenberg JJ, Hill JE: Resolution and characterization of distinct cpn60-based subgroups of Gardnerella vaginalis in the vaginal microbiota. PLoS One 2012, 7:e43009.
  • [50]dos Lopez Santos Santiago GL, Deschaght P, El AN, Kiama TN, Verstraelen H, Jefferson KK, et al.: Gardnerella vaginalis comprises three distinct genotypes of which only two produce sialidase. Am J Obstet Gynecol 2011, 204:450-7.
  • [51]O’Hanlon DE, Moench TR, Cone RA: In vaginal fluid, bacteria associated with bacterial vaginosis can be suppressed with lactic acid but not hydrogen peroxide. BMC Infect Dis 2011, 11:200. BioMed Central Full Text
  • [52]Kyongo JK, Jespers V, Goovaerts O, Michiels J, Menten J, Fichorova RN, et al.: Searching for lower female genital tract soluble and cellular biomarkers: defining levels and predictors in a cohort of healthy Caucasian women. PLoS One 2012, 7:e43951.
  • [53]Roberts CL, Rickard K, Kotsiou G, Morris JM: Treatment of asymptomatic vaginal candidiasis in pregnancy to prevent preterm birth: an open-label pilot randomized controlled trial. BMC Pregnancy Childbirth 2011, 11:18. BioMed Central Full Text
  • [54]Hilber AM, Francis SC, Chersich M, Scott P, Redmond S, Bender N, et al.: Intravaginal practices, vaginal infections and HIV acquisition: systematic review and meta-analysis. PLoS One 2010, 5:e9119.
  • [55]Low N, Chersich MF, Schmidlin K, Egger M, Francis SC, van de Wijgert JH, et al.: Intravaginal practices, bacterial vaginosis, and HIV infection in women: individual participant data meta-analysis. PLoS Med 2011, 8:e1000416.
  • [56]Hull T, Hilber AM, Chersich MF, Bagnol B, Prohmmo A, Smit JA, et al.: Prevalence, motivations, and adverse effects of vaginal practices in Africa and Asia: findings from a multicountry household survey. J Womens Health (Larchmt) 2011, 20:1097-109.
  • [57]Hernandez-Rodriguez C, Romero-Gonzalez R, Albani-Campanario M, Figueroa-Damian R, Meraz-Cruz N, Hernandez-Guerrero C: Vaginal microbiota of healthy pregnant Mexican women is constituted by four Lactobacillus species and several vaginosis-associated bacteria. Infect Dis Obstet Gynecol 2011, 2011:851485.
  • [58]Sha BE, Zariffard MR, Wang QJ, Chen HY, Bremer J, Cohen MH, 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.
  • [59]Schellenberg JJ, Links MG, Hill JE, Dumonceaux TJ, Kimani J, Jaoko W, et al.: Molecular definition of vaginal microbiota in East African commercial sex workers. Appl Environ Microbiol 2011, 77:4066-74.
  • [60]Eschenbach DA, Patton DL, Hooton TM, Meier AS, Stapleton A, Aura J, et al.: Effects of vaginal intercourse with and without a condom on vaginal flora and vaginal epithelium. J Infect Dis 2001, 183:913-8.
  • [61]Tameliene R, Barcaite E, Stoniene D, Buinauskiene J, Markuniene E, Kudreviciene A, et al.: Escherichia coli colonization in neonates: prevalence, perinatal transmission, antimicrobial susceptibility, and risk factors. Medicina (Kaunas) 2012, 48:71-6.
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