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Urinary symptoms are associated with certain urinary microbes in urogynecologic surgical patients

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A Commentary to this article was published on 17 September 2018

Abstract

Introduction and hypothesis

Persistent and de novo symptoms decrease satisfaction after urogynecologic surgery. We investigated whether the preoperative bladder microbiome is associated with urinary symptoms prior to and after urogynecologic surgery.

Methods

One hundred twenty-six participants contributed responses to the validated OABq symptom questionnaire. Catheterized (bladder) urine samples and vaginal and perineal swabs were collected immediately preoperatively. Bacterial DNA in the urine samples and swabs was sequenced and classified.

Results

Preoperative symptom severity was significantly worse in sequence-positive patients. Higher OABq Symptom Severity (OABqSS) scores (more symptomatic) were associated with higher abundance in bladder urine of two bacterial species: Atopobium vaginae and Finegoldia magna. The presence of Atopobium vaginae in bladder urine also was correlated with its presence in either the vagina or perineum.

Conclusions

Two specific bacterial species detected in bladder urine, Atopobium vaginae and Finegoldia magna, are associated with preoperative urinary symptom severity in women undergoing POP/SUI surgery. The reservoir for Atopobium vaginae may be adjacent pelvic floor niches. This observation should be validated in a larger cohort to determine whether there is a microbiologic etiology for certain preoperative urinary symptoms.

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Abbreviations

OABq :

Overactive Bladder Questionnaire

UDI :

Urinary Distress Inventory

POPDI :

Pelvic Organ Prolapse Distress Inventory

CRADI :

Colorectal Anal Distress Inventory (CRADI)

UTI :

Urinary tract infection

POP :

Pelvic organ prolapse

UI :

Urinary incontinence

BMI :

Body mass index

DNA :

Deoxyribonucleic acid

PCR :

Polymerase chain reaction

OTU :

Operational taxonomic unit

SUI :

Stress urinary incontinence

References

  1. Riemsma R, Hagen S, Kirschner-Hermanns R, Norton C, Wijk H, Andersson KE, et al. Can incontinence be cured? A systematic review of cure rates. BMC Med. 2017;15:63.

    Article  Google Scholar 

  2. Burgio KL, Brubaker L, Richter HE, Wai CY, Litman HJ, France DB, et al. Patient satisfaction with stress incontinence surgery. Neurourol Urodyn. 2010;29:1403–9.

    Article  Google Scholar 

  3. Pham T, Kenton K, Mueller E, Brubaker L. New pelvic symptoms are common after reconstructive pelvic surgery. Am J Obstet Gynecol. 2009;200:88.e81–5.

    Article  Google Scholar 

  4. Karram MM, Segal JL, Vassallo BJ, Kleeman SD. Complications and untoward effects of the tension-free vaginal tape procedure. Obstet Gynecol. 2003;101:929–32.

    PubMed  Google Scholar 

  5. Nygaard I, Brubaker L, Chai TC, Markland AD, Menefee SA, Sirls L, et al. Risk factors for urinary tract infection following incontinence surgery. Int Urogynecol J. 2011;22:1255–65.

    Article  Google Scholar 

  6. Gehrich AP, Patzwald JR, Kern ME, Squires CC, Lustik MB. The incidence of early and recurrent urinary tract infections after midurethral sling operations. Mil Med. 2014;179:1301–6.

    Article  Google Scholar 

  7. Fok CS, McKinley K, Mueller ER, Kenton K, Schreckenberger P, Wolfe A, et al. Day of surgery urine cultures identify urogynecologic patients at increased risk for postoperative urinary tract infection. J Urol. 2013;189:1721–4.

    Article  Google Scholar 

  8. Nienhouse V, Gao X, Dong Q, Nelson DE, Toh E, McKinley K, et al. Interplay between bladder microbiota and urinary antimicrobial peptides: mechanisms for human urinary tract infection risk and symptom severity. PLoS One. 2014;9:e114185.

    Article  Google Scholar 

  9. Karstens L, Asquith M, Davin S, Stauffer P, Fair D, Gregory WT, et al. Does the urinary microbiome play a role in urgency urinary incontinence and its severity? Front Cell Infect Microbiol. 2016;6:78.

    Article  Google Scholar 

  10. Pearce MM, Hilt EE, Rosenfeld AB, Zilliox MJ, Thomas-White K, Fok C, et al. The female urinary microbiome: a comparison of women with and without urgency urinary incontinence. MBio. 2014;5:e01283–14.

    Article  CAS  Google Scholar 

  11. Pearce MM, Zilliox MJ, Rosenfeld AB, Thomas-White KJ, Richter HE, Nager CW, et al. The female urinary microbiome in urgency urinary incontinence. Am J Obstet Gynecol. 2015;213:347.e341–11.

    Article  Google Scholar 

  12. Thomas-White KJ, Hilt EE, Fok C, Pearce MM, Mueller ER, Kliethermes S, et al. Incontinence medication response relates to the female urinary microbiota. Int Urogynecol J. 2016;27:723–33.

    Article  Google Scholar 

  13. Barber MD, Kuchibhatla MN, Pieper CF, Bump RC. Psychometric evaluation of 2 comprehensive condition-specific quality of life instruments for women with pelvic floor disorders. Am J Obstet Gynecol. 2001;185:1388–95.

    Article  CAS  Google Scholar 

  14. Uebersax JS, Wyman JF, Shumaker SA, McClish DK, Fantl JA. Short forms to assess life quality and symptom distress for urinary incontinence in women: the incontinence impact questionnaire and the urogenital distress inventory. Continence program for women research group. Neurourol Urodyn. 1995;14:131–9.

    Article  CAS  Google Scholar 

  15. Coyne K, Revicki D, Hunt T, Corey R, Stewart W, Bentkover J, et al. Psychometric validation of an overactive bladder symptom and health-related quality of life questionnaire: the oab-q. Qual Life Res. 2002;11:563–74.

    Article  CAS  Google Scholar 

  16. Wolfe AJ, Toh E, Shibata N, Rong R, Kenton K, Fitzgerald M, et al. Evidence of uncultivated bacteria in the adult female bladder. J Clin Microbiol. 2012;50:1376–83.

    Article  Google Scholar 

  17. Ackerman AL, Underhill DM. The mycobiome of the human urinary tract: potential roles for fungi in urology. Ann Transl Med. 2017;5:31.

    Article  Google Scholar 

  18. Hilt EE, McKinley K, Pearce MM, Rosenfeld AB, Zilliox MJ, Mueller ER, et al. Urine is not sterile: use of enhanced urine culture techniques to detect resident bacterial flora in the adult female bladder. J Clin Microbiol. 2014;52:871–6.

    Article  Google Scholar 

  19. Yuan S, Cohen DB, Ravel J, Abdo Z, Forney LJ. Evaluation of methods for the extraction and purification of DNA from the human microbiome. PLoS One. 2012;7:e33865.

    Article  CAS  Google Scholar 

  20. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009;75:7537–41.

    Article  CAS  Google Scholar 

  21. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. Uchime improves sensitivity and speed of chimera detection. Bioinformatics. 2011;27:2194–200.

    Article  CAS  Google Scholar 

  22. Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive bayesian classifier for rapid assignment of rrna sequences into the new bacterial taxonomy. Appl Environ Microbiol. 2007;73:5261–7.

    Article  CAS  Google Scholar 

  23. Gao X, Lin H, Revanna K, Dong Q. A bayesian taxonomic classification method for 16s rrna gene sequences with improved species-level accuracy. BMC Bioinformatics. 2017;18:247.

    Article  Google Scholar 

  24. Polatti F. Bacterial vaginosis, atopobium vaginae and nifuratel. Curr Clin Pharmacol. 2012;7:36–40.

    Article  CAS  Google Scholar 

  25. Knoester M, Lashley LE, Wessels E, Oepkes D, Kuijper EJ. First report of atopobium vaginae bacteremia with fetal loss after chorionic villus sampling. J Clin Microbiol. 2011;49:1684–6.

    Article  Google Scholar 

  26. Bretelle F, Rozenberg P, Pascal A, Favre R, Bohec C, Loundou A, et al. High atopobium vaginae and gardnerella vaginalis vaginal loads are associated with preterm birth. Clin Infect Dis. 2015;60:860–7.

    Article  CAS  Google Scholar 

  27. Bretelle F, Fenollar F, Baumstarck K, Fortanier C, Cocallemen JF, Serazin V, et al. Screen-and-treat program by point-of-care of atopobium vaginae and gardnerella vaginalis in preventing preterm birth (autop trial): study protocol for a randomized controlled trial. Trials. 2015;16:470.

    Article  Google Scholar 

  28. 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.

    Article  CAS  Google Scholar 

  29. 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.

    Article  CAS  Google Scholar 

  30. 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.

    Article  Google Scholar 

  31. Murphy EC, Frick IM. Gram-positive anaerobic cocci--commensals and opportunistic pathogens. FEMS Microbiol Rev. 2013;37:520–53.

    Article  CAS  Google Scholar 

  32. Fouts DE, Pieper R, Szpakowski S, Pohl H, Knoblach S, Suh MJ, et al. Integrated next-generation sequencing of 16s rdna and metaproteomics differentiate the healthy urine microbiome from asymptomatic bacteriuria in neuropathic bladder associated with spinal cord injury. J Transl Med. 2012;10:174.

    Article  CAS  Google Scholar 

  33. Khasriya R, Sathiananthamoorthy S, Ismail S, Kelsey M, Wilson M, Rohn JL, et al. Spectrum of bacterial colonization associated with urothelial cells from patients with chronic lower urinary tract symptoms. J Clin Microbiol. 2013;51:2054–62.

    Article  Google Scholar 

  34. Price TK, Dune T, Hilt EE, Thomas-White KJ, Kliethermes S, Brincat C, et al. The clinical urine culture: enhanced techniques improve detection of clinically relevant microorganisms. J Clin Microbiol. 2016;54(5):1216–1222.

    Article  CAS  Google Scholar 

  35. Coorevits L, Heytens S, Boelens J, Claeys G. The resident microflora of voided midstream urine of healthy controls: standard versus expanded urine culture protocols. Eur J Clin Microbiol Infect Dis. 2016;36(4):635–639.

    Article  Google Scholar 

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Acknowledgments

We thank Mary Tulke, RN, for her assistance with participant recruitment and sample collection. We thank Noriko Shibata, MS, for her assistance with sample analysis. We also thank Dr. Michael Zilliox and Gina Kuffel of the Loyola Genomics Facility for performing the DNA sequencing.

Funding

This study was supported by NIH grants R21 DK097435 and P20 DK108268, a Falk Foundation grant (LU#202567), and financial support from the Society of Women in Urology.

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Authors

Corresponding author

Correspondence to Linda Brubaker.

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Conflicts of interest

L. Brubaker—Editorial Stipends: Journal of American Medical Association, Female Pelvic Medicine and Reconstructive Surgery, Up To Date; Research Funding: NIH; Board Stipend: American Board of Obstetrics and Gynecology.

A. J. Wolfe—Investigator Initiated Studies: Astellas Scientific and Medical Affairs, Inc.; Kimberly Clarke Corp.

E.R. Mueller—Astellas-Advisory Board, Boston Scientific-Advisory Board.

The remaining authors claim no conflicts of interest.

Electronic supplementary material

Supplemental Figure 1.

Fifteen most abundant bacterial genera detected in catheterized urine (A), vaginal swab (B), and perineal swab (C). The top 15 most abundant bacterial genera for each body site are displayed in standard box-and-whisker plots, with the mean values in diamonds and outliers in dots. (PDF 12 kb)

Supplemental Figure 1B

(PDF 12 kb)

Supplemental Figure 1C

(PDF 12 kb)

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Fok, C.S., Gao, X., Lin, H. et al. Urinary symptoms are associated with certain urinary microbes in urogynecologic surgical patients. Int Urogynecol J 29, 1765–1771 (2018). https://doi.org/10.1007/s00192-018-3732-1

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  • DOI: https://doi.org/10.1007/s00192-018-3732-1

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