Influence of biofilms on morbidity associated with short-term indwelling ureteral stents: a prospective observational study

  • Patrick BetschartEmail author
  • Valentin Zumstein
  • Matthias T. Buhmann
  • Werner C. Albrich
  • Oliver Nolte
  • Sabine Güsewell
  • Hans-Peter Schmid
  • Qun Ren
  • Dominik Abt
Original Article



To evaluate the influence of biofilms on morbidity associated with short-term ureteral stenting using contemporary methods of biofilm examination and validated assessment of symptoms.


Patients undergoing temporary ureteral stenting for secondary ureterorenoscopy due to urinary calculi were prospectively included. The German Ureteral Stent Symptoms Questionnaire (USSQ) was used to assess stent-associated morbidity. Biofilms were removed from stents using ‘pinhole extraction’, a novel, validated, abrasion-based technique. Extracted biofilms were analyzed for total mass, bacterial load and mineral components. Correlation between total biofilm mass and USSQ total score was the primary outcome variable analyzed using Spearman correlation. Secondary outcomes included correlations between various biofilm characteristics and symptoms.


94 patients were included in the analysis. Extracted biofilm mass had a median of 37.0 mg (0–310.2 mg) per stent. No correlation between total biofilm mass and USSQ total score was found (Spearman r = 0.012; p = 0.911). Correlations between biofilm characteristics and morbidity were generally weak and not significant. Significant correlations could be found between biofilm mass and hematuria (r = 0.280; p = 0.007), and between the number of bacteria (qPCR) and the USSQ subscore for pain (r = 0.243; p = 0.019) and the intake of analgesics (r = 0.259; p = 0.012).


Based on elaborated biofilm examination methods and validated self-reported outcome measures, our findings indicate that biofilms might aggravate some lower urinary tract symptoms but are not the main trigger for stent-associated morbidity in short-term ureteral stenting.


Ureteral stent Biofilm Morbidity Ureteral Stent Symptoms Questionnaire USSQ Symptoms 



The authors would like to thank Alistair Reeves for editing the manuscript, Luzia Wiesli for technical assistance, and Antonia Neels for support with XRD analyses.

Author contributions

PB protocol/project development, data collection and management, data analysis, manuscript writing. VZ protocol/project development, data collection and management, data analysis, manuscript writing. MTB protocol/project development, data collection and management, data analysis, manuscript writing. WCA protocol/project development, data analysis, manuscript writing. ON protocol/project development, data analysis, manuscript writing. SG data analysis, manuscript writing. H-PS protocol/project development, manuscript writing. QR protocol/project development, data analysis, manuscript writing. DA protocol/project development, data collection and management, data analysis, manuscript writing.

Support/financial disclosures

The study was supported by an internal grant of Cantonal Hospital St. Gallen and the Swiss Federal Laboratories for Materials Science and Technology (Empa/KSSG 15/12).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed involving human participants were in accordance with the ethical standards of the institutional and national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.


  1. 1.
    Betschart P, Zumstein V, Piller A, Schmid HP, Abt D (2017) Prevention and treatment of symptoms associated with indwelling ureteral stents: a systematic review. Int J Urol. CrossRefPubMedGoogle Scholar
  2. 2.
    Joshi HB, Stainthorpe A, Keeley FX Jr, MacDonagh R, Timoney AG (2001) Indwelling ureteral stents: evaluation of quality of life to aid outcome analysis. J Endourol Endourol Soc 15(2):151–154. CrossRefGoogle Scholar
  3. 3.
    Walker NA, Bultitude MF, Brislane K, Thomas K, Glass JM (2014) Management of stent symptoms: what a pain! BJU Int 114(6):797–798. CrossRefPubMedGoogle Scholar
  4. 4.
    Abt D, Warzinek E, Schmid HP, Haile SR, Engeler DS (2015) Influence of patient education on morbidity caused by ureteral stents. Int J Urol 22(7):679–683. CrossRefPubMedGoogle Scholar
  5. 5.
    Denstedt JD, Cadieux PA (2009) Eliminating biofilm from ureteral stents: the Holy Grail. Curr Opin Urol 19(2):205–210. CrossRefPubMedGoogle Scholar
  6. 6.
    Pidsudko Z (2004) Distribution and chemical coding of neurons in intramural ganglia of the porcine urinary bladder trigone. Folia Histochem Cytobiol 42(1):3–11PubMedGoogle Scholar
  7. 7.
    Irani J, Siquier J, Pires C, Lefebvre O, Dore B, Aubert J (1999) Symptom characteristics and the development of tolerance with time in patients with indwelling double-pigtail ureteric stents. BJU Int 84(3):276–279CrossRefGoogle Scholar
  8. 8.
    Zumstein V, Betschart P, Albrich WC, Buhmann MT, Ren Q, Schmid HP, Abt D (2017) Biofilm formation on ureteral stents—incidence, clinical impact, and prevention. Swiss Med Wkly 147:w14408. CrossRefPubMedGoogle Scholar
  9. 9.
    Riedl CR, Plas E, Hubner WA, Zimmerl H, Ulrich W, Pfluger H (1999) Bacterial colonization of ureteral stents. Eur Urol 36(1):53–59. CrossRefPubMedGoogle Scholar
  10. 10.
    Chromek M, Slamova Z, Bergman P, Kovacs L, Podracka L, Ehren I, Hokfelt T, Gudmundsson GH, Gallo RL, Agerberth B, Brauner A (2006) The antimicrobial peptide cathelicidin protects the urinary tract against invasive bacterial infection. Nat Med 12(6):636–641. CrossRefPubMedGoogle Scholar
  11. 11.
    Poljakovic M, Svensson ML, Svanborg C, Johansson K, Larsson B, Persson K (2001) Escherichia coli-induced inducible nitric oxide synthase and cyclooxygenase expression in the mouse bladder and kidney. Kidney Int 59(3):893–904. CrossRefPubMedGoogle Scholar
  12. 12.
    Rivas-Santiago B, Serrano CJ, Enciso-Moreno JA (2009) Susceptibility to infectious diseases based on antimicrobial peptide production. Infect Immun 77(11):4690–4695. CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Bonkat G, Rieken M, Muller G, Roosen A, Siegel FP, Frei R, Wyler S, Gasser T, Bachmann A, Widmer AF (2013) Microbial colonization and ureteral stent-associated storage lower urinary tract symptoms: the forgotten piece of the puzzle? World J Urol 31(3):541–546. CrossRefPubMedGoogle Scholar
  14. 14.
    Abt D, Dotzer K, Honek P, Muller K, Engeler DS, Burger M, Schmid HP, Knoll T, Sanguedolce F, Joshi HB, Fritsche HM (2016) The German linguistic validation of the Ureteral Stent Symptoms Questionnaire (USSQ). World J Urol. CrossRefPubMedGoogle Scholar
  15. 15.
    EAU Guidelines on Urological Infections. Accessed June 2016
  16. 16.
    Buhmann MT, Abt D, Altenried S, Rupper P, Betschart P, Zumstein V, Maniura-Weber K, Ren Q (2018) Extraction of biofilms from ureteral stents for quantification and cultivation-dependent and -independent analyses. Front Microbiol 9:1470. CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Nadkarni MA, Martin FE, Jacques NA, Hunter N (2002) Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology 148(Pt 1):257–266. CrossRefPubMedGoogle Scholar
  18. 18.
    Grazulis S, Daskevic A, Merkys A, Chateigner D, Lutterotti L, Quiros M, Serebryanaya NR, Moeck P, Downs RT, Le Bail A (2012) Crystallography Open Database (COD): an open-access collection of crystal structures and platform for world-wide collaboration. Nucleic Acids Res 40 (Database Issue):D420–427.
  19. 19.
    Kawahara T, Ito H, Terao H, Yoshida M, Matsuzaki J (2012) Ureteral stent encrustation, incrustation, and coloring: morbidity related to indwelling times. J Endourol Endourol Soc 26(2):178–182. CrossRefGoogle Scholar
  20. 20.
    Abt D, Mordasini L, Warzinek E, Schmid HP, Haile SR, Engeler DS, Mullhaupt G (2015) Is intravesical stent position a predictor of associated morbidity? Korean J Urol 56(5):370–378. CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Laube N, Kleinen L, Avrutin V, Bode U, Meissner A, Fisang C (2008) The distribution of crystalline material in obstructed stents–in need for intra-luminal surface modification? J Biomed Mater Res B Appl Biomater 87(2):590–597. CrossRefPubMedGoogle Scholar
  22. 22.
    Yossepowitch O, Lifshitz DA, Dekel Y, Gross M, Keidar DM, Neuman M, Livne PM, Baniel J (2001) Predicting the success of retrograde stenting for managing ureteral obstruction. J Urol 166(5):1746–1749CrossRefGoogle Scholar
  23. 23.
    Minardi D, Montanari MP, Tili E, Cochetti I, Mingoia M, Varaldo PE, Muzzonigro G (2008) Effects of fluoroquinolones on bacterial adhesion and on preformed biofilm of strains isolated from urinary double J stents. J Chemother 20(2):195–201. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Patrick Betschart
    • 1
    Email author
  • Valentin Zumstein
    • 1
  • Matthias T. Buhmann
    • 2
  • Werner C. Albrich
    • 3
  • Oliver Nolte
    • 4
  • Sabine Güsewell
    • 5
  • Hans-Peter Schmid
    • 1
  • Qun Ren
    • 2
  • Dominik Abt
    • 1
  1. 1.Department of UrologyCantonal Hospital St. GallenSt. GallenSwitzerland
  2. 2.Laboratory for Biointerfaces, Department Materials Meet LifeEmpa, Swiss Federal Laboratories for Materials Science and TechnologySt. GallenSwitzerland
  3. 3.Division of Infectious Diseases and Hospital EpidemiologyCantonal Hospital St. GallenSt. GallenSwitzerland
  4. 4.Center for Laboratory MedicineSt. GallenSwitzerland
  5. 5.Clinical Trials UnitCantonal Hospital St. GallenSt. GallenSwitzerland

Personalised recommendations