Vaginal microbiota and human papillomavirus infection among young Swedish women.
Adolescent
Bacteria
/ classification
Cross-Sectional Studies
Female
Genotyping Techniques
High-Throughput Nucleotide Sequencing
Humans
Papillomaviridae
/ classification
Papillomavirus Infections
/ epidemiology
Papillomavirus Vaccines
/ therapeutic use
Phylogeny
Sequence Analysis, DNA
/ methods
Sweden
/ epidemiology
Vagina
/ microbiology
Young Adult
Journal
NPJ biofilms and microbiomes
ISSN: 2055-5008
Titre abrégé: NPJ Biofilms Microbiomes
Pays: United States
ID NLM: 101666944
Informations de publication
Date de publication:
12 10 2020
12 10 2020
Historique:
received:
20
03
2020
accepted:
10
09
2020
entrez:
13
10
2020
pubmed:
14
10
2020
medline:
29
5
2021
Statut:
epublish
Résumé
Human papillomavirus (HPV) infection is one of the most common sexually transmitted diseases. To define the HPV-associated microbial community among a high vaccination coverage population, we carried out a cross-sectional study with 345 young Swedish women. The microbial composition and its association with HPV infection, including 27 HPV types, were analyzed. Microbial alpha-diversity was found significantly higher in the HPV-infected group (especially with oncogenic HPV types and multiple HPV types), compared with the HPV negative group. The vaginal microbiota among HPV-infected women was characterized by a larger number of bacterial vaginosis-associated bacteria (BVAB), Sneathia, Prevotella, and Megasphaera. In addition, the correlation analysis demonstrated that twice as many women with non-Lactobacillus-dominant vaginal microbiota were infected with oncogenic HPV types, compared with L. crispatus-dominated vaginal microbiota. The data suggest that HPV infection, especially oncogenic HPV types, is strongly associated with a non-Lactobacillus-dominant vaginal microbiota, regardless of age and vaccination status.
Identifiants
pubmed: 33046723
doi: 10.1038/s41522-020-00146-8
pii: 10.1038/s41522-020-00146-8
pmc: PMC7552401
doi:
Substances chimiques
Papillomavirus Vaccines
0
Types de publication
Comparative Study
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
39Références
Bruni, L. et al. Cervical human papillomavirus prevalence in 5 continents: meta-analysis of 1 million women with normal cytological findings. J. Infect. Dis. 202, 1789–1799 (2010).
pubmed: 21067372
doi: 10.1086/657321
Smith, J. S., Melendy, A., Rana, R. K. & Pimenta, J. M. Age-specific prevalence of infection with human papillomavirus in females: a global review. J. Adolesc. Health 43, S5–S25 (2008).
pubmed: 18809145
doi: 10.1016/S1054-139X(08)00317-0
Lehtinen, M., Baussano, I., Paavonen, J., Vänskä, S. & Dillner, J. Eradication of human papillomavirus and elimination of HPV-related diseases - scientific basis for global public health policies. Expert Rev. Vaccines 18, 153–160 (2019).
pubmed: 30657348
doi: 10.1080/14760584.2019.1568876
Muñoz, N. et al. Epidemiologic classification of human papillomavirus types associated with cervical cancer. New Engl. J. Med. 348, 518–527 (2003).
pubmed: 12571259
doi: 10.1056/NEJMoa021641
Clifford, G. M., Smith, J. S., Plummer, M., Muñoz, N. & Franceschi, S. Human papillomavirus types in invasive cervical cancer worldwide: a meta-analysis. Br. J. Cancer 88, 63–73 (2003).
pubmed: 12556961
pmcid: 2376782
doi: 10.1038/sj.bjc.6600688
Du, J., Näsman, A., Carlson, J. W., Ramqvist, T. & Dalianis, T. Prevalence of human papillomavirus (HPV) types in cervical cancer 2003-2008 in Stockholm, Sweden, before public HPV vaccination. Acta Oncol. 50, 1215–1219 (2011).
pubmed: 21726177
doi: 10.3109/0284186X.2011.584556
Ährlund-Richter, A. et al. Changes in cervical human papillomavirus (HPV) prevalence at a youth clinic in stockholm, sweden, a decade after the introduction of the HPV vaccine. Front. Cell. Infect. Microbiol. 9, 59 (2019).
pubmed: 30949454
pmcid: 6435486
doi: 10.3389/fcimb.2019.00059
Grün, N. et al. Follow-up on oral and cervical human papillomavirus prevalence 2013-2015 in youth at a youth clinic in Stockholm, Sweden. Infect. Dis. 48, 169–170 (2016).
doi: 10.3109/23744235.2015.1094573
Ramqvist, T. et al. Pre-vaccination prevalence of human papillomavirus types in the genital tract of 15-23-year-old women attending a youth health clinic in Stockholm, Sweden. Scand. J. Infect. Dis. 43, 115–121 (2011).
pubmed: 20964488
doi: 10.3109/00365548.2010.526957
Chaban, B. et al. Characterization of the vaginal microbiota of healthy Canadian women through the menstrual cycle. Microbiome 2, 23 (2014).
pubmed: 25053998
pmcid: 4106219
doi: 10.1186/2049-2618-2-23
Fettweis, J. M. et al. The vaginal microbiome and preterm birth. Nat. Med. 25, 1012–1021 (2019).
pubmed: 31142849
pmcid: 6750801
doi: 10.1038/s41591-019-0450-2
Mitra, A. et al. The vaginal microbiota, human papillomavirus infection and cervical intraepithelial neoplasia: what do we know and where are we going next? Microbiome 4, 58 (2016).
pubmed: 27802830
pmcid: 5088670
doi: 10.1186/s40168-016-0203-0
Onderdonk, A. B., Delaney, M. L. & Fichorova, R. N. The human microbiome during bacterial vaginosis. Clin. Microbiol. Rev. 29, 223–238 (2016).
pubmed: 26864580
pmcid: 4786887
doi: 10.1128/CMR.00075-15
Brotman, R. M. et al. Interplay between the temporal dynamics of the vaginal microbiota and human papillomavirus detection. J. Infect. Dis. 210, 1723–1733 (2014).
pubmed: 24943724
pmcid: 4296189
doi: 10.1093/infdis/jiu330
Petrova, M. I., van den Broek, M., Balzarini, J., Vanderleyden, J. & Lebeer, S. Vaginal microbiota and its role in HIV transmission and infection. FEMS Microbiol. Rev. 37, 762–792 (2013).
pubmed: 23789590
doi: 10.1111/1574-6976.12029
DiGiulio, D. B. et al. Temporal and spatial variation of the human microbiota during pregnancy. Proc. Natl Acad. Sci. USA 112, 11060–11065 (2015).
pubmed: 26283357
doi: 10.1073/pnas.1502875112
Ravel, J. et al. Vaginal microbiome of reproductive-age women. Proc. Natl Acad. Sci. USA 108, 4680–4687 (2011).
pubmed: 20534435
doi: 10.1073/pnas.1002611107
Serrano, M. G. et al. Racioethnic diversity in the dynamics of the vaginal microbiome during pregnancy. Nat. Med. 25, 1001–1011 (2019).
pubmed: 31142850
pmcid: 6746180
doi: 10.1038/s41591-019-0465-8
Coleman, J. S. & Gaydos, C. A. Molecular diagnosis of bacterial vaginosis: an update. J. Clin. Microbiol. 56, e00342-18 (2018).
Fredricks, D. N., Fiedler, T. L. & Marrazzo, J. M. Molecular identification of bacteria associated with bacterial vaginosis. New Engl. J. Med. 353, 1899–1911 (2005).
pubmed: 16267321
doi: 10.1056/NEJMoa043802
Oakley, B. B., Fiedler, T. L., Marrazzo, J. M. & Fredricks, D. N. Diversity of human vaginal bacterial communities and associations with clinically defined bacterial vaginosis. Appl. Environ. Microbiol. 74, 4898–4909 (2008).
pubmed: 18487399
pmcid: 2519371
doi: 10.1128/AEM.02884-07
Ugur, A. R., Tuncer, E. I. & Findik, D. Identification of bacterial vaginosis-associated bacteria in male urethra: Co-occurrence of Atopobium vaginae and Gardnerella vaginalis. Marshall J. Med. https://doi.org/10.21161/mjm.180025 (2019).
Huang, X. et al. Cervicovaginal microbiota composition correlates with the acquisition of high-risk human papillomavirus types. Int. J. Cancer 143, 621–634 (2018).
pubmed: 29479697
doi: 10.1002/ijc.31342
Norenhag, J. et al. The vaginal microbiota, human papillomavirus and cervical dysplasia: a systematic review and network meta-analysis. BJOG. https://doi.org/10.1111/1471-0528.15854 (2019)
Brusselaers, N., Shrestha, S. A. D. E. E. P., van de Wijgert, J. A. N. N. E. K. E. & Verstraelen, H. A. N. S. Vaginal dysbiosis and the risk of human papillomavirus and cervical cancer: systematic review and meta-analysis. Am. J. Obstet. Gynecol. 221, 9–18 (2019).
pubmed: 30550767
doi: 10.1016/j.ajog.2018.12.011
Mitra, A. et al. The vaginal microbiota associates with the regression of untreated cervical intraepithelial neoplasia 2 lesions. Nat. Commun. 11, 1999 (2020).
pubmed: 32332850
pmcid: 7181700
doi: 10.1038/s41467-020-15856-y
Curty, G. et al. Analysis of the cervical microbiome and potential biomarkers from postpartum HIV-positive women displaying cervical intraepithelial lesions. Sci. Rep. 7, 17364 (2017).
pubmed: 29234019
pmcid: 5727204
doi: 10.1038/s41598-017-17351-9
Callahan, B. J. et al. Replication and refinement of a vaginal microbial signature of preterm birth in two racially distinct cohorts of US women. Proc. Natl Acad. Sci. USA 114, 9966–9971 (2017).
pubmed: 28847941
doi: 10.1073/pnas.1705899114
Łaniewski, P. et al. Linking cervicovaginal immune signatures, HPV and microbiota composition in cervical carcinogenesis in non-Hispanic and Hispanic women. Sci. Rep. 8, 7593 (2018).
pubmed: 29765068
pmcid: 5954126
doi: 10.1038/s41598-018-25879-7
Di Paola, M. et al. Characterization of cervico-vaginal microbiota in women developing persistent high-risk Human Papillomavirus infection. Sci. Rep. 7, 10200 (2017).
pubmed: 28860468
pmcid: 5579045
doi: 10.1038/s41598-017-09842-6
Godoy-Vitorino, F. I. L. I. P. A. et al. Cervicovaginal fungi and bacteria associated with cervical intraepithelial neoplasia and high-risk human papillomavirus infections in a hispanic population. Front. Microbiol. 9, 2533 (2018).
pubmed: 30405584
pmcid: 6208322
doi: 10.3389/fmicb.2018.02533
Shannon, B. et al. Association of HPV infection and clearance with cervicovaginal immunology and the vaginal microbiota. Mucosal Immunol. 10, 1310–1319 (2017).
pubmed: 28120845
pmcid: 5526752
doi: 10.1038/mi.2016.129
Hugerth, L. W. et al. A comprehensive automated pipeline for human microbiome sampling, 16S rRNA gene sequencing and bioinformatics processing. BioRxiv https://doi.org/10.1101/286526 (2018).
Nordfors, C. et al. Human papillomavirus prevalence is high in oral samples of patients with tonsillar and base of tongue cancer. Oral Oncol. 50, 491–497 (2014).
pubmed: 24613649
doi: 10.1016/j.oraloncology.2014.02.012
Dalianis, T. et al. Human papillomavirus DNA and p16(INK4a) expression in hypopharyngeal cancer and in relation to clinical outcome, in Stockholm, Sweden. Oral Oncol. 51, 857–861 (2015).
pubmed: 26120094
doi: 10.1016/j.oraloncology.2015.06.002
Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 17, 10 (2011).
doi: 10.14806/ej.17.1.200
Callahan, B. J. et al. DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).
pubmed: 27214047
pmcid: 27214047
doi: 10.1038/nmeth.3869
Davis, N. M., Proctor, D. M., Holmes, S. P., Relman, D. A. & Callahan, B. J. Simple statistical identification and removal of contaminant sequences in marker-gene and metagenomics data. Microbiome 6, 226 (2018).
pubmed: 30558668
pmcid: 6298009
doi: 10.1186/s40168-018-0605-2
Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596 (2013).
pubmed: 23193283
doi: 10.1093/nar/gks1219
Zhang, Z., Schwartz, S., Wagner, L. & Miller, W. A greedy algorithm for aligning DNA sequences. J. Comput. Biol. 7, 203–214 (2000).
pubmed: 10890397
doi: 10.1089/10665270050081478
NCBI Resource Coordinators. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 44, D7–D19 (2016).
doi: 10.1093/nar/gkv1290
Holm, J. B. et al. Comparative metagenome-assembled genome analysis of Lachnovaginosum genomospecies, formerly known as BVAB1. BioRxiv https://doi.org/10.1101/657197 (2019).
Austin, M. N. et al. Mageeibacillus indolicus gen. nov., sp. nov.: a novel bacterium isolated from the female genital tract. Anaerobe 32, 37–42 (2015).
pubmed: 25482717
doi: 10.1016/j.anaerobe.2014.12.003
Hyman, R. W. et al. Diversity of the vaginal microbiome correlates with preterm birth. Reprod. Sci. 21, 32–40 (2014).
pubmed: 23715799
pmcid: 3857766
doi: 10.1177/1933719113488838
Hyman, R. W. et al. Microbes on the human vaginal epithelium. Proc. Natl Acad. Sci. USA 102, 7952–7957 (2005).
pubmed: 15911771
doi: 10.1073/pnas.0503236102
Ferris, M. J., Masztal, A. & Martin, D. H. Use of species-directed 16S rRNA gene PCR primers for detection of Atopobium vaginae in patients with bacterial vaginosis. J. Clin. Microbiol. 42, 5892–5894 (2004).
pubmed: 15583334
pmcid: 535275
doi: 10.1128/JCM.42.12.5892-5894.2004
Zhou, X. et al. Differences in the composition of vaginal microbial communities found in healthy Caucasian and black women. ISME J. 1, 121–133 (2007).
pubmed: 18043622
doi: 10.1038/ismej.2007.12
Hoyles, L., Collins, M. D., Falsen, E., Nikolaitchouk, N. & McCartney, A. L. Transfer of members of the genus Falcivibrio to the genus Mobiluncus, and emended description of the genus Mobiluncus. Syst. Appl. Microbiol. 27, 72–83 (2004).
pubmed: 15053324
doi: 10.1078/0723-2020-00260
Zozaya-Hinchliffe, M., Lillis, R., Martin, D. H. & Ferris, M. J. Quantitative PCR assessments of bacterial species in women with and without bacterial vaginosis. J. Clin. Microbiol. 48, 1812–1819 (2010).
pubmed: 20305015
pmcid: 2863870
doi: 10.1128/JCM.00851-09