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Bacterial biofilm formation on vaginal ring pessaries used for pelvic organ prolapse

International Urogynecology Journal volume 33, pages 287–295 (2022)Cite this article

Abstract

Introduction and hypothesis

The objective of this study was to characterize the bacterial biofilm on vaginal ring pessaries used to treat pelvic organ prolapse and investigate the relationship between biofilm phenotype and patient symptoms and clinical signs that are suggestive of inflammation.

Methods

This was a cross-sectional observational study of 40 women wearing a ring-shaped pessary continuously for at least 12 weeks. Participants underwent a clinical examination, and the pessary was removed. Clinical signs were recorded. A swab from the pessary surface and a high vaginal swab were collected from each woman. Participants completed a questionnaire on symptoms. Pessary biofilm presence and phenotype were determined by scanning electron microscopy (SEM). Vaginal and pessary bacterial composition was determined by 16S rRNA gene sequencing. The relationship between biofilm phenotype and symptoms and clinical signs was assessed using logistic regression.

Results

SEM confirmed biofilm formation on all 40 pessaries. Microbiota data were available for 25 pessary swabs. The pessary biofilm microbiota was composed of bacteria typically found in the vagina and was categorized into Lactobacillus-dominated (n = 10/25 pessaries, 40%) communities and Lactobacillus-deficient communities with high relative abundance of anaerobic/facultative anaerobes (n = 15/25 pessaries, 60%). While increasing age was associated with presence of a Lactobacillus-deficient pessary biofilm (odds ratio = 3.60, 95% CI [1.16–11.22], p = 0.04), no associations between biofilm microbiota composition and symptoms or clinical signs were observed.

Conclusions

Lactobacillus-deficient biofilms commonly form on pessaries following long-term use. However, the contribution of biofilm phenotype to symptoms and clinical signs remains to be determined.

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References

  1. Hendrix SL, Clark A, Nygaard I, Aragaki A, Barnabei V, McTiernan A. Pelvic organ prolapse in the Women’s Health Initiative: gravity and gravidity. Am J Obstet Gynecol. 2002;186(6):1160–6. https://doi.org/10.1067/mob.2002.123819.

    Article  PubMed  Google Scholar 

  2. Olsen AL, Smith VJ, Bergstrom JO, Colling JC, Clark AL. Epidemiology of surgically managed pelvic organ prolapse and urinary incontinence. Obstet Gynecol. 1997;89(4):501–6. https://doi.org/10.1016/S0029-7844(97)00058-6.

    Article  CAS  PubMed  Google Scholar 

  3. Obstetricians ACo, Bulletins-Gynecology GCoP, Society AU. Pelvic organ prolapse: ACOG practice bulletin, number 214. Obstet Gynecol. 2019;134(5):e126–42. https://doi.org/10.1097/AOG.0000000000003519.

    Article  Google Scholar 

  4. Sarma S, Ying T, Moore KH. Long-term vaginal ring pessary use: discontinuation rates and adverse events. BJOG. 2009;116(13):1715–21. https://doi.org/10.1111/j.1471-0528.2009.02380.x.

    Article  CAS  PubMed  Google Scholar 

  5. Donlan RM. Biofilms: microbial life on surfaces. Emerg Infect Dis. 2002;8(9):881–90. https://doi.org/10.3201/eid0809.020063.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science. 1999;284(5418):1318–22. https://doi.org/10.1126/science.284.5418.1318.

    Article  CAS  PubMed  Google Scholar 

  7. Hardy L, Cerca N, Jespers V, Vaneechoutte M, Crucitti T. Bacterial biofilms in the vagina. Res Microbiol. 2017;168(9-10):865–74. https://doi.org/10.1016/j.resmic.2017.02.001.

    Article  PubMed  Google Scholar 

  8. Trautner BW, Darouiche RO. Catheter-associated infections: pathogenesis affects prevention. Arch Intern Med. 2004;164(8):842–50. https://doi.org/10.1001/archinte.164.8.842.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Swidsinski A, Mendling W, Loening-Baucke V, Swidsinski S, Dorffel Y, Scholze J, et al. An adherent Gardnerella vaginalis biofilm persists on the vaginal epithelium after standard therapy with oral metronidazole. Am J Obstet Gynecol. 2008;198(1):97 e91-96. https://doi.org/10.1016/j.ajog.2007.06.039.

    Article  CAS  Google Scholar 

  10. Kalia N, Singh J, Kaur M. Microbiota in vaginal health and pathogenesis of recurrent vulvovaginal infections: a critical review. Ann Clin Microbiol Antimicrob. 2020;19(1):5. https://doi.org/10.1186/s12941-020-0347-4.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Gunawardana M, Moss JA, Smith TJ, Kennedy S, Kopin E, Nguyen C, et al. Microbial biofilms on the surface of intravaginal rings worn in non-human primates. J Med Microbiol. 2011;60(Pt 6):828–37. https://doi.org/10.1099/jmm.0.028225-0.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Fregosi NJ, Hobson DTG, Kinman CL, Gaskins JT, Stewart JR, Meriwether KV. Changes in the vaginal microenvironment as related to frequency of pessary removal. Female Pelvic Med Reconstr Surg. 2018;24(2):166–71. https://doi.org/10.1097/SPV.0000000000000520.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Barber MD, Walters MD, Bump RC. Short forms of two condition-specific quality-of-life questionnaires for women with pelvic floor disorders (PFDI-20 and PFIQ-7). Am J Obstet Gynecol. 2005;193(1):103–13. https://doi.org/10.1016/j.ajog.2004.12.025.

    Article  CAS  PubMed  Google Scholar 

  14. Herdman M, Gudex C, Lloyd A, Janssen M, Kind P, Parkin D, et al. Development and preliminary testing of the new five-level version of EQ-5D (EQ-5D-5L). Qual Life Res. 2011;20(10):1727–36. https://doi.org/10.1007/s11136-011-9903-x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Plummer EL, Vodstrcil LA, Danielewski JA, Murray GL, Fairley CK, Garland SM, et al. Combined oral and topical antimicrobial therapy for male partners of women with bacterial vaginosis: acceptability, tolerability and impact on the genital microbiota of couples - a pilot study. PLoS One. 2018;13(1):e0190199. https://doi.org/10.1371/journal.pone.0190199.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 2011;17(1):10–2.

    Article  Google Scholar 

  17. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7(5):335–6. https://doi.org/10.1038/nmeth.f.303.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Schmieder R, Lim YW, Rohwer F, Edwards R. TagCleaner: identification and removal of tag sequences from genomic and metagenomic datasets. BMC Bioinformatics. 2010;11:341. https://doi.org/10.1186/1471-2105-11-341.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13(7):581–3. https://doi.org/10.1038/nmeth.3869.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41(Database issue):D590–6. https://doi.org/10.1093/nar/gks1219.

    Article  CAS  PubMed  Google Scholar 

  21. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2016) vegan: Community Ecology Package. R package version 2.4-1 edn.,

  22. Rohart F, Gautier B, Singh A, Le Cao KA. mixOmics: an R package for ‘omics feature selection and multiple data integration. PLoS Comput Biol. 2017;13(11):e1005752. https://doi.org/10.1371/journal.pcbi.1005752.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Hardy L, Jespers V, De Baetselier I, Buyze J, Mwambarangwe L, Musengamana V, et al. Association of vaginal dysbiosis and biofilm with contraceptive vaginal ring biomass in African women. PLoS One. 2017;12(6):e0178324. https://doi.org/10.1371/journal.pone.0178324.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Miller L, MacFarlane SA, Materi HL. A scanning electron microscopic study of the contraceptive vaginal ring. Contraception. 2005;71(1):65–7. https://doi.org/10.1016/j.contraception.2004.07.015.

    Article  CAS  PubMed  Google Scholar 

  25. Crucitti T, Hardy L, van de Wijgert J, Agaba S, Buyze J, Kestelyn E, et al. Contraceptive rings promote vaginal lactobacilli in a high bacterial vaginosis prevalence population: a randomised, open-label longitudinal study in Rwandan women. PLoS One. 2018;13(7):e0201003. https://doi.org/10.1371/journal.pone.0201003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Brotman RM, Shardell MD, Gajer P, Fadrosh D, Chang K, Silver MI, et al. Association between the vaginal microbiota, menopause status, and signs of vulvovaginal atrophy. Menopause. 2014;21(5):450–8. https://doi.org/10.1097/GME.0b013e3182a4690b.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Hillier SL, Lau RJ. Vaginal microflora in postmenopausal women who have not received estrogen replacement therapy. Clin Infect Dis. 1997;25(Suppl 2):S123–6. https://doi.org/10.1086/516221.

    Article  PubMed  Google Scholar 

  28. Heinemann C, Reid G. Vaginal microbial diversity among postmenopausal women with and without hormone replacement therapy. Can J Microbiol. 2005;51(9):777–81. https://doi.org/10.1139/w05-070.

    Article  CAS  PubMed  Google Scholar 

  29. Gliniewicz K, Schneider GM, Ridenhour BJ, Williams CJ, Song Y, Farage MA, et al. Comparison of the vaginal microbiomes of premenopausal and postmenopausal women. Front Microbiol. 2019;10:193. https://doi.org/10.3389/fmicb.2019.00193.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Alnaif B, Drutz HP. Bacterial vaginosis increases in pessary users. Int Urogynecol J Pelvic Floor Dysfunct. 2000;11(4):219–22; discussion 222-213. https://doi.org/10.1007/pl00004026.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors would like to acknowledge Saima Wani and Georgia Privato for contributions towards specimen collection and Marin Poljak for contributions towards laboratory work.

Funding

This work was supported by a grant from the Urogynaecology Special Purpose Fund, The Royal Women’s Hospital, Melbourne, Australia.

Author information

Authors and Affiliations

  1. Pelvic Floor Unit, The Royal Women’s Hospital, 20 Flemington Rd, Parkville, 3051, Australia

    Felicity G. Gould & Marcus P. Carey

  2. Centre for Women’s Infectious Diseases Research, The Royal Women’s Hospital, Parkville, Australia

    Erica L. Plummer, Gerald L. Murray, Jennifer A. Danielewski & Suzanne M. Garland

  3. Infection & Immunity Theme, Murdoch Children’s Research Institute, Parkville, Australia

    Erica L. Plummer, Gerald L. Murray, Jennifer A. Danielewski & Suzanne M. Garland

  4. Department of Obstetrics and Gynaecology, The University of Melbourne, Parkville, 3052, Australia

    Gerald L. Murray, Sepehr N. Tabrizi & Suzanne M. Garland

Authors
  1. Felicity G. Gould
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  2. Marcus P. Carey
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  3. Erica L. Plummer
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  4. Gerald L. Murray
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  5. Jennifer A. Danielewski
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  7. Suzanne M. Garland
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Contributions

F. G. Gould: Protocol/Project development, Data collection and management, Data analysis, Manuscript writing/editing.

M. P. Carey: Protocol/Project development, Manuscript writing/editing,

E. L. Plummer: Data analysis, Manuscript writing/editing.

G. L. Murray: Laboratory/experimental analysis, Manuscript writing/editing.

J. A. Danielewski: Laboratory/experimental analysis, Manuscript editing.

S. N. Tabrizi: Protocol/Project development, Manuscript editing.

S. M. Garland: Protocol/Project development, Manuscript editing.

Corresponding author

Correspondence to Felicity G. Gould.

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Supplementary Information

ESM 1

(PDF 24 kb)

ESM 2

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Figure S1

The microbiota composition of all pessary (blue) and vaginal specimens included in this study. The heatmap displays the relative abundance of the 15 most abundant taxa detected in all specimens. Hierarchical clustering of Jaccard distances with Ward linkage was used to generate the heatmap and demonstrates similarity of microbiota composition between specimens. The metadata above the heatmap indicate the participant ID and sample type (pessary and vaginal). Pessary and vaginal samples collected from the same woman frequently appear next to each other in the heatmap, indicating similarity in microbiota composition at the two sites. (PDF 28 kb)

Figure S2

Principal component analysis of pessary (blue) and vaginal (orange) samples included in this study. Pessary and vaginal samples collected from the same woman frequently cluster together (or overlap) in the plot, indicating similarity in microbiota composition at the two sites. Pessary samples are labeled with P followed by the study ID and vaginal samples are labeled with V followed by the study ID (i.e., P1 and V1 represent the pessary and vaginal samples collected from participant 1, respectively). (PDF 5 kb)

ESM 5

(DOCX 19 kb)

ESM 6

(DOCX 18 kb)

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Gould, F.G., Carey, M.P., Plummer, E.L. et al. Bacterial biofilm formation on vaginal ring pessaries used for pelvic organ prolapse. Int Urogynecol J 33, 287–295 (2022). https://doi.org/10.1007/s00192-021-04717-x

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  • DOI: https://doi.org/10.1007/s00192-021-04717-x

Keywords

  • Bacterial biofilm
  • Vaginal ring pessary
  • Pelvic organ prolapse
  • Vaginal microbiota
  • Pessary microbiota
  • Scanning electron microscopic