دورية أكاديمية
Cervicovaginal bacterial communities in reproductive-aged Tanzanian women with Schistosoma mansoni, Schistosoma haematobium, or without schistosome infection.
| العنوان: | Cervicovaginal bacterial communities in reproductive-aged Tanzanian women with Schistosoma mansoni, Schistosoma haematobium, or without schistosome infection. |
|---|---|
| المؤلفون: | Bullington BW; Center for Global Health, Weill Cornell Medicine, New York, NY, USA. bbullington@unc.edu., Lee MH; Center for Global Health, Weill Cornell Medicine, New York, NY, USA., Mlingi J; Bugando Medical Centre, Mwanza, Tanzania., Paul N; Bugando Medical Centre, Mwanza, Tanzania., Aristide C; Center for Global Health, Weill Cornell Medicine, New York, NY, USA., Fontana E; Lucille Castori Center for Microbes, Inflammation and Cancer, Memorial Sloan Kettering Cancer Center, New York, NY, USA., Littmann ER; Duchossosis Family Institute, University of Chicago, Chicago, IL, USA., Mukerebe C; National Institute for Medical Research, Mwanza, Tanzania., Shigella P; National Institute for Medical Research, Mwanza, Tanzania., Kashangaki P; National Institute for Medical Research, Mwanza, Tanzania., Kalluvya SE; Bugando Medical Centre, Mwanza, Tanzania., de Dood CJ; Department of Cell and Chemical Biology, Leiden University Medical Center, Leiden, Netherlands., van Dam GJ; Department of Cell and Chemical Biology, Leiden University Medical Center, Leiden, Netherlands., Corstjens PLAM; Department of Parasitology, Leiden University Medical Center, Leiden, Netherlands., Fitzgerald DW; Center for Global Health, Weill Cornell Medicine, New York, NY, USA., Pamer EG; Duchossosis Family Institute, University of Chicago, Chicago, IL, USA., Downs JA; Center for Global Health, Weill Cornell Medicine, New York, NY, USA. |
| المصدر: | The ISME journal [ISME J] 2021 May; Vol. 15 (5), pp. 1539-1550. Date of Electronic Publication: 2021 Jan 06. |
| نوع المنشور: | Journal Article; Research Support, N.I.H., Extramural; Research Support, Non-U.S. Gov't |
| اللغة: | English |
| بيانات الدورية: | Publisher: Nature Pub. Group Country of Publication: England NLM ID: 101301086 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1751-7370 (Electronic) Linking ISSN: 17517362 NLM ISO Abbreviation: ISME J Subsets: MEDLINE |
| أسماء مطبوعة: | Original Publication: London : Nature Pub. Group |
| مواضيع طبية MeSH: | Schistosomiasis haematobia*/epidemiology , Schistosomiasis mansoni*, Adult ; Animals ; Bacteria/genetics ; Female ; Humans ; RNA, Ribosomal, 16S/genetics ; Schistosoma haematobium ; Schistosoma mansoni/genetics |
| مستخلص: | Schistosome infection is recognized as a potentially modifiable risk factor for HIV in women by the World Health Organization. Alterations in cervicovaginal bacteria have been associated with HIV acquisition and have not been studied in schistosome infection. We collected cervical swabs from Tanzanian women with and without S. mansoni and S. haematobium to determine effects on cervicovaginal microbiota. Infected women were treated, and follow-up swabs were collected after 3 months. 16S rRNA sequencing was performed on DNA extracted from swabs. We compared 39 women with S. mansoni with 52 uninfected controls, and 16 with S. haematobium with 27 controls. S. mansoni-infected women had increased abundance of Peptostreptococcus (p = 0.026) and presence of Prevotella timonesis (p = 0.048) compared to controls. High-intensity S. haematobium infection was associated with more diverse cervicovaginal bacterial communities than uninfected controls (p = 0.0159). High-intensity S. mansoni infection showed a similar trend (p = 0.154). At follow-up, we observed increased alpha diversity in S. mansoni (2.53 vs. 1.72, p = 0.022) and S. haematobium (2.05 vs. 1.12, p = 0.066) infection groups compared to controls. Modifications in cervicovaginal microbiota, particularly increased diversity and abundance of taxa associated with bacterial vaginosis and HIV (Peptostreptococcus, Prevotella), were associated with schistosome infection. |
| References: | Kjetland EF, Ndhlovu PD, Gomo E, Mduluza T, Midzi N, Gwanzura L, et al. Association between genital schistosomiasis and HIV in rural Zimbabwean women. AIDS. 2006;20:593–600. (PMID: 1647012410.1097/01.aids.0000210614.45212.0a) Downs JA, Mguta C, Kaatano GM, Mitchell KB, Bang H, Simplice H, et al. Urogenital schistosomiasis in women of reproductive age in Tanzania’s Lake Victoria region. Am J Trop Med Hyg. 2011;84:364–9. (PMID: 21363971304280910.4269/ajtmh.2011.10-0585) Brodish PH, Singh K. Association between schistosoma haematobium exposure and human immunodeficiency virus infection among females in Mozambique. Am J Trop Med Hyg. 2016;94:1040–4. (PMID: 26976893485660010.4269/ajtmh.15-0652) Downs JA, van Dam GJ, Changalucha JM, Corstjens PLAM, Peck RN, de Dood CJ, et al. Association of Schistosomiasis and HIV infection in Tanzania. Am J Trop Med Hyg. 2012;87:868–73. (PMID: 23033399351626210.4269/ajtmh.2012.12-0395) Downs JA, Dupnik KM, van Dam GJ, Urassa M, Lutonja P, Kornelis D, et al. Effects of schistosomiasis on susceptibility to HIV-1 infection and HIV-1 viral load at HIV-1 seroconversion: a nested case-control study. PLoS Negl Trop Dis. 2017;11:e0005968. (PMID: 28945756562902810.1371/journal.pntd.0005968) Wall KM, Kilembe W, Vwalika B, Dinh C, Livingston P, Lee Y-M, et al. Schistosomiasis is associated with incident HIV transmission and death in Zambia. PLoS Negl Trop Dis. 2018;12:e0006902. (PMID: 30543654629256410.1371/journal.pntd.0006902) Ssetaala A, Nakiyingi-Miiro J, Asiki G, Kyakuwa N, Mpendo J, Van Dam GJ, et al. Schistosoma mansoni and HIV acquisition in fishing communities of Lake Victoria, Uganda: a nested case-control study. Trop Med Int Health. 2015;20:1190–5. (PMID: 25940951452948210.1111/tmi.12531) Bochner AF, Baeten JM, Secor WE, Dam GJ, Szpiro AA, Njenga SM, et al. Associations between schistosomiasis and HIV‐1 acquisition risk in four prospective cohorts: a nested case‐control analysis. J Int AIDS Soc. 2020;23:e25534. (PMID: 32585078731639010.1002/jia2.25534) World Health Organization. Schistosomiasis. World Health Organization. 2020. https://www.who.int/news-room/fact-sheets/detail/schistosomiasis . UNAIDS. The need for a holistic approach to women and HIV | UNAIDS. UNAIDS. 2020. https://www.unaids.org/en/resources/presscentre/featurestories/2018/march/20180316_holistic-approach-to-women-and-hiv . Downs JA, de Dood CJ, Dee HE, McGeehan M, Khan H, Marenga A, et al. Schistosomiasis and human immunodeficiency virus in men in Tanzania. Am J Trop Med Hyg. 2017;96:856–62. (PMID: 281676005392632) Dupnik K, Lee M, Mishra P, Reust M, Colombe S, Haider S, et al. Altered cervical mucosal gene expression and lower IL-15 levels in women with S. haematobium but not S. mansoni infection. J Infect Dis. 2019; 219:1777–85. (PMID: 3059073610.1093/infdis/jiy742) Gosmann C, Anahtar MN, Handley SA, Farcasanu M, Abu-Ali G, Bowman BA, et al. Lactobacillus-deficient cervicovaginal bacterial communities are associated with increased HIV acquisition in young South African women. Immunity. 2017;46:29–37. (PMID: 28087240527062810.1016/j.immuni.2016.12.013) Anahtar M, Byrne E, Doherty K, Bowman B, Yamamoto H, Soumillon M, et al. Cervicovaginal bacteria are a major modulator of host inflammatory responses in the female genital tract. Immunity. 2015;42:965–76. (PMID: 25992865446136910.1016/j.immuni.2015.04.019) Masson L, Passmore J-AS, Liebenberg LJ, Werner L, Baxter C, Arnold KB. et al. Genital inflammation and the risk of HIV acquisition in women. Clin Infect Dis. 2015;61:260. (PMID: 25900168456599510.1093/cid/civ298) Jenkins TP, Peachey LE, Ajami NJ, MacDonald AS, Hsieh MH, Brindley PJ, et al. Schistosoma mansoni infection is associated with quantitative and qualitative modifications of the mammalian intestinal microbiota. Sci Rep. 2018;8:12072. (PMID: 30104612608995710.1038/s41598-018-30412-x) Schneeberger PHH, Coulibaly JT, Panic G, Daubenberger C, Gueuning M, Frey JE, et al. Investigations on the interplays between Schistosoma mansoni, praziquantel and the gut microbiome. Parasit Vectors. 2018;11:168. (PMID: 29530088584856510.1186/s13071-018-2739-2) Kay GL, Millard A, Sergeant MJ, Midzi N, Gwisai R, Mduluza T, et al. Differences in the Faecal microbiome in schistosoma haematobium infected children vs. uninfected children. PLoS Negl Trop Dis. 2015;9:e0003861. (PMID: 26114287448274410.1371/journal.pntd.0003861) Ajibola O, Rowan AD, Ogedengbe CO, Mshelia MB, Cabral DJ, Eze AA, et al. Urogenital schistosomiasis is associated with signatures of microbiome dysbiosis in Nigerian adolescents. Sci Rep. 2019;9:829. (PMID: 30696838635165810.1038/s41598-018-36709-1) Adebayo AS, Suryavanshi MV, Bhute S, Agunloye AM, Isokpehi RD, Anumudu CI, et al. The microbiome in urogenital schistosomiasis and induced bladder pathologies. PLoS Negl Trop Dis. 2017;11:e0005826. (PMID: 28793309556518910.1371/journal.pntd.0005826) Gelfand M, Ross MD, Blair DM, Weber MC. Distribution and extent of schistosomiasis in female pelvic organs, with special reference to the genital tract, as determined at autopsy. Am J Trop Med Hyg. 1971;20:846–9. (PMID: 513169310.4269/ajtmh.1971.20.846) Mishra P, Colombe S, Paul N, Mlingi J, Tosiri I, Aristide C, et al. Insufficiency of annual praziquantel treatment to control Schistosoma mansoni infections in adult women: a longitudinal cohort study in rural Tanzania. PLoS Negl Trop Dis. 2019;13:e0007844. (PMID: 31751333689489010.1371/journal.pntd.0007844) Berhe N, Medhin G, Erko B, Smith T, Gedamu S, Bereded D, et al. Variations in helminth faecal egg counts in Kato-Katz thick smears and their implications in assessing infection status with Schistosoma mansoni. Acta Trop. 2004;92:205–12. (PMID: 1553328810.1016/j.actatropica.2004.06.011) Corstjens PLAM, van Lieshout L, Zuiderwijk M, Kornelis D, Tanke HJ, Deelder AM, et al. Up-converting phosphor technology-based lateral flow assay for detection of Schistosoma circulating anodic antigen in serum. J Clin Microbiol. 2008;46:171–6. (PMID: 1794264510.1128/JCM.00877-07) Corstjens PLAM, De Dood CJ, Kornelis D, Fat EMTK, Wilson RA, Kariuki TM, et al. Tools for diagnosis, monitoring and screening of Schistosoma infections utilizing lateral-flow based assays and upconverting phosphor labels. Parasitology. 2014;141:1841–55. (PMID: 2493259510.1017/S0031182014000626) Ministry of Health and Social Welfare. The national road map strategic plan to accelerate reduction of maternal, newborn and child deaths in Tanzania (2016-2020). Dar es Salaam: Ministry of Health and Social Welfare; 2015. Sorbara MT, Dubin K, Littmann ER, Moody TU, Fontana E, Seok R, et al. Inhibiting antibiotic-resistant Enterobacteriaceae by microbiota-mediated intracellular acidification. J Exp Med. 2019;216:84–98. (PMID: 30563917631452410.1084/jem.20181639) Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 2012;6:1621–4. (PMID: 22402401340041310.1038/ismej.2012.8) Edgar R. Local homology recognition and distance measures in linear time using compressed amino acid alphabets. Nucleic Acids Res. 2004;32:380–5. (PMID: 1472992237329010.1093/nar/gkh180) Price JT, Vwalika B, Hobbs M, Nelson JAE, Stringer EM, Zou F, et al. Highly diverse anaerobe-predominant vaginal microbiota among HIV-infected pregnant women in Zambia. PLoS One. 2019;14:e0223128. (PMID: 31577818677452610.1371/journal.pone.0223128) Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R, et al. Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods. 2013;10:57–59. (PMID: 2320243510.1038/nmeth.2276) Navas-Molina JA, Peralta-Sánchez JM, González A, McMurdie PJ, Vázquez-Baeza Y, Xu Z, et al. Advancing our understanding of the human microbiome using QIIME. Method Enzymol. 2013;531:371–444. (PMID: 10.1016/B978-0-12-407863-5.00019-8) Callahan BJ, Sankaran K, Fukuyama JA, McMurdie PJ, Holmes SP. Bioconductor Workflow for microbiome data analysis: from raw reads to community analyses. F1000Research. 2016;5:1492. (PMID: 27508062495502710.12688/f1000research.8986.2) Kaul A, Mandal S, Davidov O, Peddada SD. Analysis of microbiome data in the presence of excess zeros. Front Microbiol. 2017;8:2114. (PMID: 29163406568200810.3389/fmicb.2017.02114) McClelland RS, Lingappa JR, Srinivasan S, Kinuthia J, John-Stewart GC, Jaoko W, et al. Evaluation of the association between the concentrations of key vaginal bacteria and the increased risk of HIV acquisition in African women from five cohorts: a nested case-control study. Lancet Infect Dis. 2018;18:554–64. (PMID: 29396006644555210.1016/S1473-3099(18)30058-6) Knight R, Vrbanac A, Taylor BC, Aksenov A, Callewaert C, Debelius J, et al. Best practices for analysing microbiomes. Nat Rev Microbiol. Nat Publ Group 2018;16:410–22. Li H. Microbiome, metagenomics, and high-dimensional compositional data analysis. Annu Rev Stat Its Appl. 2015;2:73–94. (PMID: 10.1146/annurev-statistics-010814-020351) Polman K, De Vlas SJ, Gryseels B, Deelder AM. Relating serum circulating anodic antigens to faecal egg counts in Schistosoma mansoni infections: A modelling approach. Parasitology. 2000;121:601–10. (PMID: 1115593110.1017/S0031182000006843) Borgdorff H, Tsivtsivadze E, Verhelst R, Marzorati M, Jurriaans S, Ndayisaba GF, et al. Lactobacillus-dominated cervicovaginal microbiota associated with reduced HIV/STI prevalence and genital HIV viral load in african women. ISME J. 2014;8:1781–93. (PMID: 24599071413971910.1038/ismej.2014.26) Nelson TM, Borgogna JLC, Brotman RM, Ravel J, Walk ST, Yeoman CJ. Vaginal biogenic amines: biomarkers of bacterial vaginosis or precursors to vaginal dysbiosis? Front Physiol. 2015;6:253. (PMID: 26483694458643710.3389/fphys.2015.00253) Myer L, Kuhn L, Stein ZA, Wright TC, Denny L. Intravaginal practices, bacterial vaginosis, and women’s susceptibility to HIV infection: Epidemiological evidence and biological mechanisms. Lancet Infect Dis. 2005;5:786–94. (PMID: 1631015010.1016/S1473-3099(05)70298-X) Lai SK, Hida K, Shukair S, Wang Y-Y, Figueiredo A, Cone R, et al. Human immunodeficiency virus type 1 is trapped by acidic but not by neutralized human Cervicovaginal Mucus. J Virol. 2009;83:11196–11200. (PMID: 19692470277278810.1128/JVI.01899-08) Taha TE, Hoover DR, Dallabetta GA, Kumwenda NI, Mtimavalye LAR, Yang LP, et al. Bacterial vaginosis and disturbances of vaginal flora: association with increased acquisition of HIV. AIDS. 1998;12:1699–706. (PMID: 976479110.1097/00002030-199813000-00019) Martin HL, Richardson BA, Nyange PM, Lavreys L, Hillier SL, Chohan B, et al. Vaginal lactobacilli, microbial flora, and risk of human immunodeficiency virus type 1 and sexually transmitted disease acquisition. J Infect Dis. 1999;180:1863–8. (PMID: 1055894210.1086/315127) Mikamo H, Kawazoe K, Izumi K, Ito K, Katoh N, Watanabe K, et al. Bacteriological epidemiology and treatment of bacterial vaginosis. Chemotherapy. 1996;42:78–84. (PMID: 875127010.1159/000239425) Agnew A, Fulford AJ, Mwanje MT, Gachuhi K, Gutsmann V, Krijger FW, et al. Age-dependent reduction of schistosome fecundity in Schistosoma haematobium but not Schistosoma mansoni infections in humans. Am J Trop Med Hyg. 1996;55:338–43. (PMID: 884212610.4269/ajtmh.1996.55.338) Cheever AW, Kamel IA, Elwi AM, Mosimann JE, Danner R. Schistosoma mansoni and S. haematobium infections in Egypt. II. Quant parasitological Find necropsy Am J Trop Med Hyg. 1977;26:702–16. (PMID: 10.4269/ajtmh.1977.26.702) Muller R. Worms and human disease. 2nd ed. CABI Publishing;UK 2001. Turner JD, Narang P, Coles MCMA. Blood flukes exploit Peyer’s Patch lymphoid tissue to facilitate transmission from the mammalian host. Plos Pathog 2012;8:e1003063. (PMID: 23308064353437610.1371/journal.ppat.1003063) Wilson MS, Mentink-Kane MM, Pesce JT, Ramalingam TR, Thompson R, Wynn TA. Immunopathology of schistosomiasis. 2007;85:148–54. |
| معلومات مُعتمدة: | 2017067 United States DDCF_ Doris Duke Charitable Foundation; K23 AI110238 United States AI NIAID NIH HHS; P30 CA008748 United States CA NCI NIH HHS; K23 AI 110238 United States NH NIH HHS |
| فهرسة مساهمة: | Keywords: Cervicovaginal microbiota; HIV; Microbiome; Schistosomiasis; Tanzania |
| المشرفين على المادة: | 0 (RNA, Ribosomal, 16S) |
| تواريخ الأحداث: | Date Created: 20210107 Date Completed: 20210602 Latest Revision: 20230128 |
| رمز التحديث: | 20240829 |
| مُعرف محوري في PubMed: | PMC8115289 |
| DOI: | 10.1038/s41396-020-00868-9 |
| PMID: | 33408370 |
| قاعدة البيانات: | MEDLINE |
Find this article in full text from Springer Verlag. 
Full Text Finder | تدمد: | 1751-7370 |
|---|---|
| DOI: | 10.1038/s41396-020-00868-9 |