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Systematic review

Vol. 147 No. 0506 (2017)

Biofilm formation on ureteral stents – incidence, clinical impact and prevention

Cite this as:
Swiss Med Wkly. 2017;147:w14408
Published
03.02.2017

Summary

Ureteral stents are a simple, minimally invasive method of maintaining ureteral drainage to assure renal function, treat pain caused by ureteral obstruction and avoid external or visible devices. Ureteral stenting is, however, associated with a clear side-effect profile, including irritation on voiding, pain and haematuria. Complications such as stent dysfunction and clinically significant urinary tract infections are also regularly observed. Although this has not yet thoroughly researched, it appears that biofilm formation on ureteral stents plays a key role in the associated morbidity. In this review, we summarise the current evidence and identify areas that should be further studied to reduce the morbidity associated with ureteral stenting.

References

  1. Liatsikos E, Kallidonis P, Stolzenburg JU, Karnabatidis D. Ureteral stents: past, present and future. Expert Rev Med Devices. 2009;6(3):313–24. doi:.https://doi.org/10.1586/erd.09.5
  2. Joshi HB, Stainthorpe A, Keeley FX, Jr, MacDonagh R, Timoney AG. Indwelling ureteral stents: evaluation of quality of life to aid outcome analysis. J Endourol. 2001;15(2):151–4. doi:.https://doi.org/10.1089/089277901750134421
  3. Leibovici D, Cooper A, Lindner A, Ostrowsky R, Kleinmann J, Velikanov S, et al. Ureteral stents: morbidity and impact on quality of life. Isr Med Assoc J. 2005;7(8):491–4.
  4. Staubli SE, Mordasini L, Engeler DS, Sauter R, Schmid HP, Abt D. Economic Aspects of Morbidity Caused by Ureteral Stents. Urol Int. 2016;97(1):91–7. doi:.https://doi.org/10.1159/000443379
  5. Joshi HB, Newns N, Stainthorpe A, MacDonagh RP, Keeley FX, Jr, Timoney AG. Ureteral stent symptom questionnaire: development and validation of a multidimensional quality of life measure. J Urol. 2003;169(3):1060–4. doi:.https://doi.org/10.1097/01.ju.0000049198.53424.1d
  6. Lamb AD, Vowler SL, Johnston R, Dunn N, Wiseman OJ. Meta-analysis showing the beneficial effect of α-blockers on ureteric stent discomfort. BJU Int. 2011;108(11):1894–902. doi:.https://doi.org/10.1111/j.1464-410X.2011.10170.x
  7. Park SC, Jung SW, Lee JW, Rim JS. The effects of tolterodine extended release and alfuzosin for the treatment of double-j stent-related symptoms. J Endourol. 2009;23(11):1913–7. doi:.https://doi.org/10.1089/end.2009.0173
  8. Abt D, Warzinek E, Schmid HP, Haile SR, Engeler DS. Influence of patient education on morbidity caused by ureteral stents. Int J Urol. 2015;22(7):679–83. doi:.https://doi.org/10.1111/iju.12782
  9. Abt D, Mordasini L, Warzinek E, Schmid HP, Haile SR, Engeler DS, et al. Is intravesical stent position a predictor of associated morbidity? Korean J Urol. 2015;56(5):370–8. doi:.https://doi.org/10.4111/kju.2015.56.5.370
  10. Giannarini G, Keeley FX, Jr, Valent F, Manassero F, Mogorovich A, Autorino R, et al. Predictors of morbidity in patients with indwelling ureteric stents: results of a prospective study using the validated Ureteric Stent Symptoms Questionnaire. BJU Int. 2011;107(4):648–54. doi:.https://doi.org/10.1111/j.1464-410X.2010.09482.x
  11. Walker NA, Bultitude MF, Brislane K, Thomas K, Glass JM. Management of stent symptoms: what a pain! BJU Int. 2014;114(6):797–8. doi:.https://doi.org/10.1111/bju.12534
  12. Tenke P, Köves B, Nagy K, Hultgren SJ, Mendling W, Wullt B, et al. Update on biofilm infections in the urinary tract. World J Urol. 2012;30(1):51–7. doi:.https://doi.org/10.1007/s00345-011-0689-9
  13. Farsi HMA, Mosli HA, Al-Zemaity MF, Bahnassy AA, Alvarez M. Bacteriuria and colonization of double-pigtail ureteral stents: long-term experience with 237 patients. J Endourol. 1995;9(6):469–72. doi:.https://doi.org/10.1089/end.1995.9.469
  14. Riedl CR, Plas E, Hübner WA, Zimmerl H, Ulrich W, Pflüger H. Bacterial colonization of ureteral stents. Eur Urol. 1999;36(1):53–9. doi:.https://doi.org/10.1159/000019927
  15. Moher D, Liberati A, Tetzlaff J, Altman DG, Group P. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. J Clin Epidemiol. 2009;62(10):1006–12. doi:.https://doi.org/10.1016/j.jclinepi.2009.06.005
  16. Tenke P, Kovacs B, Jäckel M, Nagy E. The role of biofilm infection in urology. World J Urol. 2006;24(1):13–20. doi:.https://doi.org/10.1007/s00345-005-0050-2
  17. Venkatesan N, Shroff S, Jeyachandran K, Doble M. Effect of uropathogens on in vitro encrustation of polyurethane double J ureteral stents. Urol Res. 2011;39(1):29–37. doi:.https://doi.org/10.1007/s00240-010-0280-7
  18. Elwood CN, Lo J, Chou E, Crowe A, Arsovska O, Adomat H, et al. Understanding urinary conditioning film components on ureteral stents: profiling protein components and evaluating their role in bacterial colonization. Biofouling. 2013;29(9):1115–22. doi:.https://doi.org/10.1080/08927014.2013.829049
  19. Canales BK, Higgins L, Markowski T, Anderson L, Li QA, Monga M. Presence of five conditioning film proteins are highly associated with early stent encrustation. J Endourol. 2009;23(9):1437–42. doi:.https://doi.org/10.1089/end.2009.0389
  20. Santin M, Motta A, Denyer SP, Cannas M. Effect of the urine conditioning film on ureteral stent encrustation and characterization of its protein composition. Biomaterials. 1999;20(13):1245–51. doi:.https://doi.org/10.1016/S0142-9612(99)00026-5
  21. Busscher HJ, van der Mei HC, Schakenraad JM. Analogies in the two-dimensional spatial arrangement of adsorbed proteins and adhering bacteria: bovine serum albumin and Streptococcus sanguis 12. J Biomater Sci Polym Ed. 1992;3(1):85–94. doi:.https://doi.org/10.1163/156856292X00097
  22. Choong S, Whitfield H. Biofilms and their role in infections in urology. BJU Int. 2000;86(8):935–41. doi:.https://doi.org/10.1046/j.1464-410x.2000.00949.x
  23. Jones DS, Djokic J, Gorman SP. Characterization and optimization of experimental variables within a reproducible bladder encrustation model and in vitro evaluation of the efficacy of urease inhibitors for the prevention of medical device-related encrustation. J Biomed Mater Res B Appl Biomater. 2006;76B(1):1–7. doi:.https://doi.org/10.1002/jbm.b.30230
  24. Hedelin H. Uropathogens and urinary tract concretion formation and catheter encrustations. Int J Antimicrob Agents. 2002;19(6):484–7. doi:.https://doi.org/10.1016/S0924-8579(02)00095-X
  25. Boddicker JD, Anderson RA, Jagnow J, Clegg S. Signature-tagged mutagenesis of Klebsiella pneumoniae to identify genes that influence biofilm formation on extracellular matrix material. Infect Immun. 2006;74(8):4590–7. doi:.https://doi.org/10.1128/IAI.00129-06
  26. Schroll C, Barken KB, Krogfelt KA, Struve C. Role of type 1 and type 3 fimbriae in Klebsiella pneumoniae biofilm formation. BMC Microbiol. 2010;10(1):179. doi:.https://doi.org/10.1186/1471-2180-10-179
  27. Ong CL, Ulett GC, Mabbett AN, Beatson SA, Webb RI, Monaghan W, et al. Identification of type 3 fimbriae in uropathogenic Escherichia coli reveals a role in biofilm formation. J Bacteriol. 2008;190(3):1054–63. doi:.https://doi.org/10.1128/JB.01523-07
  28. Petrova OE, Sauer K. Sticky situations: key components that control bacterial surface attachment. J Bacteriol. 2012;194(10):2413–25. doi:.https://doi.org/10.1128/JB.00003-12
  29. Jacobsen SM, Shirtliff ME. Proteus mirabilis biofilms and catheter-associated urinary tract infections. Virulence. 2011;2(5):460–5. doi:.https://doi.org/10.4161/viru.2.5.17783
  30. Armbruster CE, Smith SN, Yep A, Mobley HL. Increased incidence of urolithiasis and bacteremia during Proteus mirabilis and Providencia stuartii coinfection due to synergistic induction of urease activity. J Infect Dis. 2014;209(10):1524–32. doi:.https://doi.org/10.1093/infdis/jit663
  31. Hola V, Peroutkova T, Ruzicka F. Virulence factors in Proteus bacteria from biofilm communities of catheter-associated urinary tract infections. FEMS Immunol Med Microbiol. 2012;65(2):343–9. doi:.https://doi.org/10.1111/j.1574-695X.2012.00976.x
  32. Holling N, Lednor D, Tsang S, Bissell A, Campbell L, Nzakizwanayo J, et al. Elucidating the genetic basis of crystalline biofilm formation in Proteus mirabilis. Infect Immun. 2014;82(4):1616–26. doi:.https://doi.org/10.1128/IAI.01652-13
  33. Jones SM, Yerly J, Hu Y, Ceri H, Martinuzzi R. Structure of Proteus mirabilis biofilms grown in artificial urine and standard laboratory media. FEMS Microbiol Lett. 2007;268(1):16–21. doi:.https://doi.org/10.1111/j.1574-6968.2006.00587.x
  34. d’Enfert C, Janbon G. Biofilm formation in Candida glabrata: What have we learnt from functional genomics approaches? FEMS Yeast Res. 2016;16(1):fov111. doi:.https://doi.org/10.1093/femsyr/fov111
  35. Fattahi S, Kafil HS, Nahai MR, Asgharzadeh M, Nori R, Aghazadeh M. Relationship of biofilm formation and different virulence genes in uropathogenic Escherichia coli isolates from Northwest Iran. GMS Hyg Infect Control. 2015;10:Doc11.
  36. Hadjifrangiskou M, Gu AP, Pinkner JS, Kostakioti M, Zhang EW, Greene SE, et al. Transposon mutagenesis identifies uropathogenic Escherichia coli biofilm factors. J Bacteriol. 2012;194(22):6195–205. doi:.https://doi.org/10.1128/JB.01012-12
  37. Newman JA, Rodrigues C, Lewis RJ. Molecular basis of the activity of SinR protein, the master regulator of biofilm formation in Bacillus subtilis. J Biol Chem. 2013;288(15):10766–78. doi:.https://doi.org/10.1074/jbc.M113.455592
  38. Orme R, Douglas CW, Rimmer S, Webb M. Proteomic analysis of Escherichia coli biofilms reveals the overexpression of the outer membrane protein OmpA. Proteomics. 2006;6(15):4269–77. doi:.https://doi.org/10.1002/pmic.200600193
  39. Orlando F, Ghiselli R, Cirioni O, Minardi D, Tomasinsig L, Mocchegiani F, et al. BMAP-28 improves the efficacy of vancomycin in rat models of gram-positive cocci ureteral stent infection. Peptides. 2008;29(7):1118–23. doi:.https://doi.org/10.1016/j.peptides.2008.03.005
  40. Schembri MA, Klemm P. Biofilm formation in a hydrodynamic environment by novel fimh variants and ramifications for virulence. Infect Immun. 2001;69(3):1322–8. doi:.https://doi.org/10.1128/IAI.69.3.1322-1328.2001
  41. Girish Kumar CP, Menon T. Biofilm production by clinical isolates of Candida species. Med Mycol. 2006;44(1):99–101. doi:.https://doi.org/10.1080/13693780500338084
  42. Marcus RJ, Post JC, Stoodley P, Hall-Stoodley L, McGill RL, Sureshkumar KK, et al. Biofilms in nephrology. Expert Opin Biol Ther. 2008;8(8):1159–66. doi:.https://doi.org/10.1517/14712598.8.8.1159
  43. Mathé L, Van Dijck P. Recent insights into Candida albicans biofilm resistance mechanisms. Curr Genet. 2013;59(4):251–64. doi:.https://doi.org/10.1007/s00294-013-0400-3
  44. Negri M, Silva S, Breda D, Henriques M, Azeredo J, Oliveira R. Candida tropicalis biofilms: effect on urinary epithelial cells. Microb Pathog. 2012;53(2):95–9. doi:.https://doi.org/10.1016/j.micpath.2012.05.006
  45. Nett JE, Andes DR. Fungal Biofilms: In Vivo Models for Discovery of Anti-Biofilm Drugs. Microbiol Spectr 3 (2015).
  46. Carugo D, Elmahdy M, Zhao X, Drake MJ, Zhang X, Clavica F. An artificial model for studying fluid dynamics in the obstructed and stented ureter. Conf Proc IEEE Eng Med Biol Soc. 2013;2013:5335–8.
  47. Clavica F, Zhao X, ElMahdy M, Drake MJ, Zhang X, Carugo D. Investigating the flow dynamics in the obstructed and stented ureter by means of a biomimetic artificial model. PLoS One. 2014;9(2):e87433. doi:.https://doi.org/10.1371/journal.pone.0087433
  48. Gorman SP, Garvin CP, Quigley F, Jones DS. Design and validation of a dynamic flow model simulating encrustation of biomaterials in the urinary tract. J Pharm Pharmacol. 2003;55(4):461–8. doi:.https://doi.org/10.1211/002235702856
  49. Robert M, Boularan AM, El Sandid M, Grasset D. Double-J ureteric stent encrustations: clinical study on crystal formation on polyurethane stents. Urol Int. 1997;58(2):100–4. doi:.https://doi.org/10.1159/000282959
  50. Shaheen T, Edirisinghe T, Gabriel M, Bourdoumis A, Buchholz N, Knight M. In vitro encrustation of a semi-permanent polymer-covered nitinol ureter stent: an artificial urine model. Urolithiasis. 2014;42(3):203–7. doi:.https://doi.org/10.1007/s00240-014-0652-5
  51. Tunney MM, Keane PF, Jones DS, Gorman SP. Comparative assessment of ureteral stent biomaterial encrustation. Biomaterials. 1996;17(15):1541–6. doi:.https://doi.org/10.1016/0142-9612(96)89780-8
  52. Waters SL, Heaton K, Siggers JH, Bayston R, Bishop M, Cummings LJ, et al. Ureteric stents: investigating flow and encrustation. Proc Inst Mech Eng H. 2008;222(4):551–61. doi:.https://doi.org/10.1243/09544119JEIM317
  53. Paick SH, Park HK, Oh SJ, Kim HH. Characteristics of bacterial colonization and urinary tract infection after indwelling of double-J ureteral stent. Urology. 2003;62(2):214–7. doi:.https://doi.org/10.1016/S0090-4295(03)00325-X
  54. Lojanapiwat B. Colonization of internal ureteral stent and bacteriuria. World J Urol. 2006;24(6):681–3. doi:.https://doi.org/10.1007/s00345-006-0135-6
  55. Kawahara T, Ito H, Terao H, Yoshida M, Matsuzaki J. Ureteral stent encrustation, incrustation, and coloring: morbidity related to indwelling times. J Endourol. 2012;26(2):178–82. doi:.https://doi.org/10.1089/end.2011.0385
  56. Rahman MA, Alam MM, Shamsuzzaman SM, Haque ME. Evaluation of bacterial colonization and bacteriuria secondary to internal ureteral stent. Mymensingh Med J. 2010;19(3):366–71.
  57. Bultitude MF, Tiptaft RC, Glass JM, Dasgupta P. Management of encrusted ureteral stents impacted in upper tract. Urology. 2003;62(4):622–6. doi:.https://doi.org/10.1016/S0090-4295(03)00506-5
  58. Kehinde EO, Rotimi VO, Al-Awadi KA, Abdul-Halim H, Boland F, Al-Hunayan A, et al. Factors predisposing to urinary tract infection after J ureteral stent insertion. J Urol. 2002;167(3):1334–7. doi:.https://doi.org/10.1016/S0022-5347(05)65294-9
  59. Sighinolfi MC, Sighinolfi GP, Galli E, Micali S, Ferrari N, Mofferdin A, et al. Chemical and Mineralogical Analysis of Ureteral Stent Encrustation and Associated Risk Factors. Urology. 2015;86(4):703–6. doi:.https://doi.org/10.1016/j.urology.2015.05.015
  60. Laube N, Kleinen L, Avrutin V, Böde U, Meissner A, Fisang C. The distribution of crystalline material in obstructed stents--in need for intra-luminal surface modification? J Biomed Mater Res B Appl Biomater. 2008;87B(2):590–7. doi:.https://doi.org/10.1002/jbm.b.31132
  61. Bithelis G, Bouropoulos N, Liatsikos EN, Perimenis P, Koutsoukos PG, Barbalias GA. Assessment of encrustations on polyurethane ureteral stents. J Endourol. 2004;18(6):550–6. doi:.https://doi.org/10.1089/end.2004.18.550
  62. Rouprêt M, Daudon M, Hupertan V, Gattegno B, Thibault P, Traxer O. Can ureteral stent encrustation analysis predict urinary stone composition? Urology. 2005;66(2):246–51. doi:.https://doi.org/10.1016/j.urology.2005.03.054
  63. Brotherhood H, Lange D, Chew BH. Advances in ureteral stents. Transl Androl Urol. 2014;3(3):314–9.
  64. Choe HS, Son SW, Choi HA, Kim HJ, Ahn SG, Bang JH, et al. Analysis of the distribution of bacteria within urinary catheter biofilms using four different molecular techniques. Am J Infect Control. 2012;40(9):e249–54. doi:.https://doi.org/10.1016/j.ajic.2012.05.010
  65. Keane PF, Bonner MC, Johnston SR, Zafar A, Gorman SP. Characterization of biofilm and encrustation on ureteric stents in vivo. Br J Urol. 1994;73(6):687–91. doi:.https://doi.org/10.1111/j.1464-410X.1994.tb07557.x
  66. Aydin HR, Irkilata L, Aydin M, Gorgun S, Demirel HC, Adanur S, et al. Incidence of bacterial colonisation after indwelling of double-J ureteral stent. Arch Ital Urol Androl. 2016;87(4):291–4. doi:.https://doi.org/10.4081/aiua.2015.4.291
  67. Kehinde EO, Rotimi VO, Al-Hunayan A, Abdul-Halim H, Boland F, Al-Awadi KA. Bacteriology of urinary tract infection associated with indwelling J ureteral stents. J Endourol. 2004;18(9):891–6. doi:.https://doi.org/10.1089/end.2004.18.891
  68. Høiby N, Bjarnsholt T, Moser C, Bassi GL, Coenye T, Donelli G, et al.; ESCMID Study Group for Biofilms and Consulting External Expert Werner Zimmerli. ESCMID guideline for the diagnosis and treatment of biofilm infections 2014. Clin Microbiol Infect. 2015;21(Suppl 1):S1–25. doi:.https://doi.org/10.1016/j.cmi.2014.10.024
  69. Bonkat G, Braissant O, Rieken M, Müller G, Frei R, van der Merwe A, et al. Comparison of the roll-plate and sonication techniques in the diagnosis of microbial ureteral stent colonisation: results of the first prospective randomised study. World J Urol. 2013;31(3):579–84. doi:.https://doi.org/10.1007/s00345-012-0963-5
  70. Wilks SA, Fader MJ, Keevil CW. Novel Insights into the Proteus mirabilis Crystalline Biofilm Using Real-Time Imaging. PLoS One. 2015;10(10):e0141711. doi:.https://doi.org/10.1371/journal.pone.0141711
  71. Bader MJ, Zilinberg K, Weidlich P, Waidelich R, Püls M, Gratzke C, et al. Encrustation of urologic double pigtail catheters-an ex vivo optical coherence tomography (OCT) study. Lasers Med Sci. 2013;28(3):919–24. doi:.https://doi.org/10.1007/s10103-012-1177-1
  72. Bonkat G, Rieken M, Müller G, Roosen A, Siegel FP, Frei R, et al. Microbial colonization and ureteral stent-associated storage lower urinary tract symptoms: the forgotten piece of the puzzle? World J Urol. 2013;31(3):541–6. doi:.https://doi.org/10.1007/s00345-012-0849-6
  73. El-Nahas AR, El-Assmy AM, Shoma AM, Eraky I, El-Kenawy MR, El-Kappany HA. Self-retaining ureteral stents: analysis of factors responsible for patients’ discomfort. J Endourol. 2006;20(1):33–7. doi:.https://doi.org/10.1089/end.2006.20.33
  74. Ben-Meir D, Golan S, Ehrlich Y, Livne PM. Characteristics and clinical significance of bacterial colonization of ureteral double-J stents in children. J Pediatr Urol. 2009;5(5):355–8. doi:.https://doi.org/10.1016/j.jpurol.2009.01.001
  75. Al-Ghazo MA, Ghalayini IF, Matani YS, El-Radaideh KM, Haddad HI. The risk of bacteriuria and ureteric stent colonization in immune-compromised patients with double J stent insertion. Int Urol Nephrol. 2010;42(2):343–7. doi:.https://doi.org/10.1007/s11255-009-9607-0
  76. Yeniyol CO, Tuna A, Yener H, Zeyrek N, Tilki A, Coskuner A. Bacterial colonization of double J stents and bacteriuria frequency. Int Urol Nephrol. 2002;34(2):199–202. doi:.https://doi.org/10.1023/A:1023285422278
  77. Akay AF, Aflay U, Gedik A, Sa̧hin H, Bircan MK. Risk factors for lower urinary tract infection and bacterial stent colonization in patients with a double J ureteral stent. Int Urol Nephrol. 2007;39(1):95–8. doi:.https://doi.org/10.1007/s11255-006-9150-1
  78. Coskun AK, Harlak A, Ozer T, Eyitilen T, Yigit T, Demirbaş S, et al. Is removal of the stent at the end of 2 weeks helpful to reduce infectious or urologic complications after renal transplantation? Transplant Proc. 2011;43(3):813–5. doi:.https://doi.org/10.1016/j.transproceed.2010.11.016
  79. Ahallal Y, Khallouk A, El Fassi MJ, Farih MH. Risk factor analysis and management of ureteral double-j stent complications. Rev Urol. 2010;12(2-3):e147–51.
  80. Singh I, Gupta NP, Hemal AK, Aron M, Seth A, Dogra PN. Severely encrusted polyurethane ureteral stents: management and analysis of potential risk factors. Urology. 2001;58(4):526–31. doi:.https://doi.org/10.1016/S0090-4295(01)01317-6
  81. Minardi D, Montanari MP, Tili E, Cochetti I, Mingoia M, Varaldo PE, et al. Effects of fluoroquinolones on bacterial adhesion and on preformed biofilm of strains isolated from urinary double J stents. J Chemother. 2008;20(2):195–201. doi:.https://doi.org/10.1179/joc.2008.20.2.195
  82. Balagué C, Fernández L, Pérez J, Grau R. Effect of ciprofloxacin on adhesive properties of non-P mannose-resistant uropathogenic Escherichia coli isolates. J Antimicrob Chemother. 2003;51(2):401–4. doi:.https://doi.org/10.1093/jac/dkg048
  83. Reid G, Habash M, Vachon D, Denstedt J, Riddell J, Beheshti M. Oral fluoroquinolone therapy results in drug adsorption on ureteral stents and prevention of biofilm formation. Int J Antimicrob Agents. 2001;17(4):317–9, discussion 319–20. doi:.https://doi.org/10.1016/S0924-8579(00)00353-8
  84. Wojnicz D, Tichaczek-Goska D, Kicia M. Pentacyclic triterpenes combined with ciprofloxacin help to eradicate the biofilm formed in vitro by Escherichia coli. Indian J Med Res. 2015;141(3):343–53. doi:.https://doi.org/10.4103/0971-5916.156631
  85. El-Feky MA, El-Rehewy MS, Hassan MA, Abolella HA, Abd El-Baky RM, Gad GF. Effect of ciprofloxacin and N-acetylcysteine on bacterial adherence and biofilm formation on ureteral stent surfaces. Pol J Microbiol. 2009;58(3):261–7.
  86. Davies DG, Marques CN. A fatty acid messenger is responsible for inducing dispersion in microbial biofilms. J Bacteriol. 2009;191(5):1393–403. doi:.https://doi.org/10.1128/JB.01214-08
  87. Al-Bareeq R. Denstedt J.D. Urinary Tract Stone Disease. London: Springer; 2011. pp 543–551.
  88. Lennon GM, Thornhill JA, Sweeney PA, Grainger R, McDermott TE, Butler MR. ‘Firm’ versus ‘soft’ double pigtail ureteric stents: a randomised blind comparative trial. Eur Urol. 1995;28(1):1–5.
  89. Lange D, Chew BH. Update on ureteral stent technology. Ther Adv Urol. 2009;1(3):143–8. doi:.https://doi.org/10.1177/1756287209341306
  90. Rosman BM, Barbosa JA, Passerotti CP, Cendron M, Nguyen HT. Evaluation of a novel gel-based ureteral stent with biofilm-resistant characteristics. Int Urol Nephrol. 2014;46(6):1053–8. doi:.https://doi.org/10.1007/s11255-013-0636-3
  91. Gabi M, Hefermehl L, Lukic D, Zahn R, Vörös J, Eberli D. Electrical microcurrent to prevent conditioning film and bacterial adhesion to urological stents. Urol Res. 2011;39(2):81–8. doi:.https://doi.org/10.1007/s00240-010-0284-3
  92. Chakravarti A, Gangodawila S, Long MJ, Morris NS, Blacklock AR, Stickler DJ. An electrified catheter to resist encrustation by Proteus mirabilis biofilm. J Urol. 2005;174(3):1129–32. doi:.https://doi.org/10.1097/01.ju.0000168618.79096.cb
  93. Tenke P, Riedl CR, Jones GL, Williams GJ, Stickler D, Nagy E. Bacterial biofilm formation on urologic devices and heparin coating as preventive strategy. Int J Antimicrob Agents. 2004;23(Suppl 1):S67–74. doi:.https://doi.org/10.1016/j.ijantimicag.2003.12.007
  94. Cauda F, Cauda V, Fiori C, Onida B, Garrone E. Heparin coating on ureteral Double J stents prevents encrustations: an in vivo case study. J Endourol. 2008;22(3):465–72. doi:.https://doi.org/10.1089/end.2007.0218
  95. Lange D, Chew BH. in Biomaterials and Tissue Engineering in Urology 85-103 (Elsevier Ltd., 2009).
  96. Stickler DJ, Evans A, Morris N, Hughes G. Strategies for the control of catheter encrustation. Int J Antimicrob Agents. 2002;19(6):499–506. doi:.https://doi.org/10.1016/S0924-8579(02)00091-2
  97. John T, Rajpurkar A, Smith G, Fairfax M, Triest J. Antibiotic pretreatment of hydrogel ureteral stent. J Endourol. 2007;21(10):1211–6. doi:.https://doi.org/10.1089/end.2007.9904
  98. Laube N, Kleinen L, Bradenahl J, Meissner A. Diamond-like carbon coatings on ureteral stents--a new strategy for decreasing the formation of crystalline bacterial biofilms? J Urol. 2007;177(5):1923–7. doi:.https://doi.org/10.1016/j.juro.2007.01.016
  99. Mendez-Probst CE, Goneau LW, MacDonald KW, Nott L, Seney S, Elwood CN, et al. The use of triclosan eluting stents effectively reduces ureteral stent symptoms: a prospective randomized trial. BJU Int. 2012;110(5):749–54. doi:.https://doi.org/10.1111/j.1464-410X.2011.10903.x
  100. Cirioni O, Ghiselli R, Silvestri C, Minardi D, Gabrielli E, Orlando F, et al. Effect of the combination of clarithromycin and amikacin on Pseudomonas aeruginosa biofilm in an animal model of ureteral stent infection. J Antimicrob Chemother. 2011;66(6):1318–23. doi:.https://doi.org/10.1093/jac/dkr107
  101. Cirioni O, Silvestri C, Ghiselli R, Kamysz W, Minardi D, Castelli P, et al. In vitro and in vivo effects of sub-MICs of pexiganan and imipenem on Pseudomonas aeruginosa adhesion and biofilm development. Infez Med. 2013;21(4):287–95.
  102. Darouiche RO, Mansouri MD, Gawande PV, Madhyastha S. Efficacy of combination of chlorhexidine and protamine sulphate against device-associated pathogens. J Antimicrob Chemother. 2008;61(3):651–7. doi:.https://doi.org/10.1093/jac/dkn006
  103. Watterson JD, Cadieux PA, Beiko DT, Cook AJ, Burton JP, Harbottle RR, et al. Oxalate-degrading enzymes from Oxalobacter formigenes: a novel device coating to reduce urinary tract biomaterial-related encrustation. J Endourol. 2003;17(5):269–74. doi:.https://doi.org/10.1089/089277903322145431
  104. Francesko A, Fernandes MM, Ivanova K, Amorim S, Reis RL, Pashkuleva I, et al. Bacteria-responsive multilayer coatings comprising polycationic nanospheres for bacteria biofilm prevention on urinary catheters. Acta Biomater. 2016;33:203–12. doi:.https://doi.org/10.1016/j.actbio.2016.01.020