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Characterizing the Urobiome in Geriatric Males with Chronic Indwelling Urinary Catheters: An Exploratory Longitudinal Study - Beyond the Abstract

Placement of long-term indwelling catheters significantly increases the risk of bladder infection. These infections, known as catheter-associated urinary tract infections (CAUTI), are widely considered to occur when the catheter is contaminated by bacteria from exogenous sources, such as the gastrointestinal tract.1 Thus, many assume the indwelling catheter takes on a passive role as a conduit between the outside world and the sterile bladder environment. Unfortunately, this dogmatic concept completely ignores the presence of resident bladder bacterial communities (microbiota).

Since the discovery of bladder microbiota in asymptomatic, presumably healthy, adult females2 and males,3,4 individual bacterial species have been associated with various bladder disease states in both sexes.5-11 Additionally, it was found that the urethra in females12 and males3,4 contains its own distinct microbiota that are also implicated in certain disease states. Thus, the microbiota of the urogenital tract (which includes the bladder, urethra, and skin outside the urethral opening) should be regarded similarly to microbiota in other body sites: these microbiota are likely key players in urogenital health and disease.

Recent evidence suggests this is also true in the context of CAUTI. In 2016, it was discovered that the human bladder’s natural response to urinary catheter placement, namely the secretion of fibrinogen, promotes bacterial colonization of the catheter.13 Moreover, persistent catheter colonization appears to rely on initial colonization by certain bacterial species.14,15 Because these bacterial species are often present in urogenital samples, the idea that resident urogenital microbiota plays a key role in CAUTI development cannot be ignored.

Our research team and others believe it is impossible to fully understand CAUTI etiology while ignoring the contribution of the urogenital microbiota to disease development. This current study was an attempt to detect changes in urogenital microbiota composition preceding CAUTI diagnosis. While this question could not be sufficiently addressed, we observed that catheter-associated microbiota are distinct and these communities are not static; instead, they are prone to bacterial fluctuations and blooms inherent to any microbiome. The main factor that distinguishes the urogenital microbiomes of chronic indwelling urinary catheter patients from other cohorts is the ubiquitous presence and high abundance of pathogenic organisms in the absence of urinary symptoms. Despite the lack of symptoms, clinical detection of pathogenic species resulted in CAUTI diagnosis and antibiotic treatment; however, these species were not eradicated. The lack of urinary symptoms and resilience to antibiotic treatment necessitate a closer look at the virulence potential of these presumed pathogens within the context of these microbiome compositions.

When considered together, these data raise two crucial questions:

  1. Could a patient’s baseline urogenital microbiota predispose them to CAUTI development?t
  2. Does the detection of any pathogenic species warrant CAUTI diagnosis or, in the absence of urinary symptoms, do these opportunistic species simply represent an alternative state for the patient’s urogenital microbiome?
Written by: Baylie R. Hochstedler-Kramer,1 Emma Stewart,1 Mark Khemanni,1 Nina M. Clark,2,3 Jorge P. Parada,2,3 Ahmer Farooq,4 Chirag Doshi,4 Alan J. Wolfe,1,3 Fritzie S. Albarillo2,3

  1. Department of Microbiology and Immunology, Stritch School of Medicine, Loyola University Chicago, Maywood, Illinois, USA.
  2. Division of Infectious Diseases, Loyola University Medical Center, Maywood, Illinois, USA.
  3. Infectious Disease and Immunology Research Institute, Loyola University Chicago, Maywood, Illinois, USA.
  4. Department of Urology, Loyola University Medical Center, Maywood, Illinois, USA.
References:

  1. Tambyah PA, Halvorson KT, Maki DG. 1999. A prospective study of pathogenesis of catheter-associated urinary tract infections. Mayo Clin Proc 74:131–136. doi: 10.4065/74.2.131
  2. Wolfe AJ, Toh E, Shibatat N, et al. Evidence of uncultivated bacteria in the adult female bladder. J Clin Microbiol. 2012; 50:1376-1383.
  3. Dong Q, Nelson DE, Toh E, et al. The microbial communities in male first catch urine are highly similar to those in paired urethral swab specimens. PLoS One. 2011; 6:e19709.
  4. Nelson DE, Dong Q, Van der Pol B, et al. Bacterial communities of the coronal sulcus and distal urethra of adolescent males. PLoS One. 2012; 7:e36298.
  5. Fouts DE, Pieper R, Szpakowski S, 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.
  6. Brubaker L, Nager CW, Richter HE, et al. Urinary bacteria in adult women with urgency urinary incontinence. Int Urogynecol J. 2014; 25:1179-1184.
  7. Pearce MM, Hilt EE, Rosenfeld AB, et al. The female urinary microbiome: a comparison of women with and without urgency urinary incontinence. MBio. 2014; 5:e01283-e01214.
  8. Khasriya R, Sathiananthamoorthy S, Ismail S, et al. Spectrum of bacterial colonization associated with urothelial cells from patients with chronic lower urinary tract symptoms. J Clin Microbiol. 2013; 51:2054-2062.
  9. Siddiqui H, Nederbragt AJ, Lagesen K, et al. Assessing diversity of the female urine microbiota by high throughput sequencing of 16S rDNA amplicons. BMC Microbiol. 2011; 11:244.
  10. Pearce MM, Zilliox MJ, Rosenfeld AB, et al. The female urinary microbiome in urgency urinary incontinence. Am J Obstet Gynecol. 2015; 213:347e1-11.
  11. Thomas-White KJ, Hilt EE, Fok C, et al. Incontinence medication response relates to the female urinary microbiota. Int Urogynecol J. 2016; 27:723-733.
  12. Chen YB, Hochstedler B, Pham TT, Acevedo-Alvarez M, Mueller ER, Wolfe AJ. 2020. The urethral microbiota: a missing link in the female urinary microbiota. J Urol 204:303–309. doi: 10.1097/JU.0000000000000910.
  13. Flores-Mireles AL, Walker JN, Bauman TM, Potretzke AM, Schreiber HL 4th, Park AM, Pinkner JS, Caparon MG, Hultgren SJ, Desai A. Fibrinogen Release and Deposition on Urinary Catheters Placed during Urological Procedures. J Urol. 2016 Aug;196(2):416-421. doi: 10.1016/j.juro.2016.01.100. Epub 2016 Jan 28. PMID: 26827873; PMCID: PMC4965327.
  14. Xu, W., Flores-Mireles, A.L., Cusumano, Z.T. et al. Host and bacterial proteases influence biofilm formation and virulence in a murine model of enterococcal catheter-associated urinary tract infection. npj Biofilms Microbiomes 3, 28 (2017). doi: 10.1038/s41522-017-0036-z
  15. Gaston, J., Andersen, MJ., Johnson, A., White, A., Humby, M., Brauer, A., Learman, B., Flores-Mireles AL. and C. E. Armbruster. Proteus mirabilis and Enterococcus faecalis persistently co-colonize the catheterized urinary tract and form recalcitrant polymicrobial biofilms with altered biofilm architecture. Pathogens. 2020, 9(10): 835. doi: 10.3390/pathogens9100835
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