World J Urol

DOI 10.1007/s00345-011-0689-9

TOPIC PAPER

Update on bioWlm infections in the urinary tract

Peter Tenke · Béla Köves · Károly Nagy · Scott J. Hultgren · Werner Mendling · Björn Wullt · Magnus Grabe · Florian M. E. Wagenlehner · Mete Cek · Robert Pickard · Henry Botto · Kurt G. Naber · Truls E. Bjerklund Johansen

Received: 2 March 2011 / Accepted: 22 April 2011© Springer-Verlag 2011

AbstractPurpose BioWlm infections have a major role in implantsor devices placed in the human body. As part of the endou-rological development, a great variety of foreign bodieshave been designed, and with the increasing number of bio-material devices used in urology, bioWlm formation anddevice infection is an issue of growing importance.Methods A literature search was performed in the Med-line database regarding bioWlm formation and the role ofbioWlms in urogenital infections using the following itemsin diVerent combinations: “bioWlm,” “urinary tract infec-tion,” “bacteriuria,” “catheter,” “stent,” and “encrustation.”The studies were graded using the Oxford Centre for Evi-dence-based Medicine classiWcation.

Results The authors present an update on the mechanismof bioWlm formation in the urinary tract with specialemphasis on the role of bioWlms in lower and upper urinarytract infections, as well as on bioWlm formation on foreignbodies, such as catheters, ureteral stents, stones, implants,and artiWcial urinary sphincters. The authors also summa-rize the diVerent methods developed to prevent bioWlm for-mation on urinary foreign bodies.Conclusions Several diVerent approaches are being inves-tigated for preventing bioWlm formation, and some promis-ing results have been obtained. However, an ideal methodhas not been developed. Future researches have to aim atidentifying eVective mechanisms for controlling bioWlmformation and to develop antimicrobial agents eVectiveagainst bacteria in bioWlms.

P. Tenke (&) · B. Köves · K. NagyDepartment of Urology, South-Pest Hospital, 1 Koves Str., 1204 Budapest, Hungarye-mail: tenke.peter@jahndelpest.hu

S. J. HultgrenDepartment of Molecular Microbiology, Washington University Medical School, St. Louis, MO 63011, USA

W. MendlingClinics of Obstetrics and Gynecology, Vivantes Klinikum Am Urban, DieVenbachstr. 1, 10967 Berlin, Germany

B. Wullt · M. GrabeDepartment of Urology, Malmö University Hospital, Lund University, 224 01 Malmö, Sweden

F. M. E. WagenlehnerClinic for Urology, Pediatric Urology and Andrology, Justus-Liebig-University, Rudolf-Buchheim-Str., 735392 Giessen, Germany

M. CekTrakya Medical Faculty, Department of Urology, 22030 Edirne, Turkey

R. PickardDepartment of Urology, Freeman Hospital, Newcastle Upon Tyne NE7 7DN, UK

H. BottoService d’urologie, Hôpital Foch, 40, rue Worth, 92151 Suresnes, France

K. G. NaberTechnical University of Munich, Arcisstrasse 21, 80333 Munich, Germany

T. E. Bjerklund JohansenDepartment of Urology, Århus University Hospital, Skejby, Brendstrupgårdsvej 100, 8200 Århus N, Denmark

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Keywords BioWlm · Urinary tract infection · Catheter · Encrustation

Introduction

By deWnition, a bioWlm is an accumulation of microorgan-isms and their extracellular products forming a structuredcommunity on a surface. BioWlm formation has a majorimpact on foreign bodies or devices placed in the humanbody. In the last decades, as part of the process of endouro-logical development a great variety of foreign bodies havebeen invented, and with the steadily increasing number ofbiomaterial devices used in urology, bioWlm formation anddevice infection is an issue of growing importance.

Methods

We performed a literature search using Medline and theCochrane Library from 1985 until February 2011, using thefollowing items in diVerent combinations: “bioWlm,” “uri-nary tract infection,” “bacteriuria,” “catheter,” “stent,”“encrustation.” A total of 1,350 publications were identi-Wed. The identiWed articles were screened by title andabstract, and 95 were found to be relevant. A review of thebibliographies of the retrieved articles was performed toidentify additional references. A total of 34 publicationswere selected in our update. The studies were rated accord-ing to the level of evidence based on the Oxford Centre forEvidence-based Medicine adaptation of the work of theAgency for Health Care Policy and Research. The manu-script was in part published originally in: Naber KG, Scha-eVer AJ, Heyns CF, Matsumoto T, Shoskes DA, BjerklundJohansen TE (eds): Urogenital Infections. European Asso-ciation of Urology—International Consultation on Urologi-cal Diseases, 1st edition 2010, Arnhem, The Netherlands,ISBN:978-90-79754-41-0.

Mechanism of bioWlm formation

A bioWlm is a structured community of microorganismsencapsulated within a self-developed polymeric matrix andadherent to a living or inert surface. The initial event in theformation of a bioWlm is the deposition of urinary compo-nents on the biomaterial leading to the formation of a con-ditioning Wlm. After insertion into the body Tamm-Horsfallglycoprotein, ions, polysaccharides, and other componentsdiVuse toward the implant prior to the arrival of the Wrstorganisms. Many of the molecules are proteinaceous, andthese proteins provide receptor sites for bacterial adhesinsthat facilitate adherence. Thus, the creation of a conditioning

Wlm alters the surface characteristics of implants. It is forthis reason that implants with altered surface characteristicscan be ineVective as mechanisms of preventing microbialattachment. The role of the conditioning Wlm is vital asmany pathogens do not have mechanisms to adhere directlyonto bare implant surfaces.

The next step is the approach and attachment of microor-ganisms. In order for bacteria to react to a surface, they mustbe able to “sense” their proximity to these surfaces. Plank-tonic bacterial cells release protons and signaling moleculeswhich diVuse radially away from the Xoating cell if not adja-cent to any surface. But a higher concentration can developclose to any surface because diVusion is limited on this side.This allows the cell to sense that it is near a surface, follow-ing which it may commit to the active process of adhesion.The initial adhesion is reversible and involves hydrophobicand electrostatic forces, followed by irreversible attachmentprovided by bacterial polysaccharides.

The Wnal stage is the formation of a bioWlm structure. Adeveloped bioWlm consists of groups of microorganismsseparated by interstitial spaces that are Wlled with surround-ing Xuid. The basic structural unit of the bioWlm is themicrocolony, which may be composed of 10–25% cells and75–90% exopolysaccharide (EPS) matrix depending on thespecies involved. The bioWlm also contains water channelswhich allow transporting of essential nutrients and oxygenfor the growth of the cells [1]. A developed bioWlm is builtup of three layers:

1. linking Wlm which attaches to the surface of tissue orbiomaterials

2. base Wlm of compact microorganisms3. surface Wlm as an outer layer, where planktonic organ-

isms can be released free-Xoating and spreading overthe surface.

The eVect of antimicrobials on bacteria in bioWlm

Antimicrobial agents eVective against planktonic bacteriafrequently fail to eradicate bacterial bioWlms. The problemis that choosing of antibiotics is based on bacterial culturesderived from planktonic bacteria which diVer in behaviorand in phenotypic form from bacteria in bioWlm. The failureof antimicrobial agents to treat bioWlms has been associatedwith a variety of mechanisms [2]:

– Agents often fail to penetrate the full depth of the bioWlm(extrinsic resistance).

– Organisms in the bioWlm grow more slowly; therefore,they are more resistant to antimicrobial agents thatrequire active growth.

– Antimicrobial binding proteins are poorly expressed inthese bacteria.

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– Bacteria within a bioWlm activate many genes that alterthe cell envelope, the molecular targets, and the suscepti-bility to antimicrobial agents (intrinsic resistance).

– Bacteria in a bioWlm can survive in the presence of anti-microbial agents at a concentration 1,000–1,500 timeshigher than the concentration needed to kill planktoniccells of the same species.

Aminoglycosides and beta-lactam antibiotics were shownto be able to prevent the formation of “young” bioWlms,while Xuoroquinolones are eVective in case of both“young” and “older” bioWlms because of their good pene-trative qualities. They are present in bioWlms even one ortwo weeks after the end of the antibiotic treatment [3, 4].

Most researchers believe that antibiotics can only slowdown the progress of bioWlm formation by eliminatingunprotected planktonic bacteria. However, during an acutefebrile phase of a bioWlm infection, antimicrobial therapy issensible and essential because the planktonic and not thebioWlm bacteria are responsible for febrile reactions.

The role of bioWlms in urinary tract infections

Chronic bacterial prostatitis

Although the classiWcation of chronic prostatitis has beenstandardized, the diVerentiation of chronic non-bacterialfrom bacterial inXammation is still challenging. The pros-tatic ducts and acini provide safe circumstances to plank-tonic bacteria to multiply and induce a host response. Atthis point, it is still relatively easy to eradicate them. How-ever, if the bacteria persist they can form sporadic bacterialmicrocolonies adherent to the epithelium of the ductal sys-tem and provoke persistent immunological stimulation andsubsequent chronic inXammation (LoE 2b) [5]. The diagno-sis of chronic bacterial prostatitis can be diYcult as colo-nized bacteria will not get into the prostatic secretion orurine sample. Antimicrobial therapy eradicates the plank-tonic bacteria but not the adherent bacterial bioWlms deepwithin the prostate gland.

Intracellular bacterial communities in recurrent cystitis

The exact mechanism of bacterial adherence and survival inthe urinary tract is not well understood. UropathogenicE. coli (UPEC) pathogenesis initiates bacterial binding tosuperWcial bladder epithelial cells, which respond to invad-ing bacteria in part by recognizing diVerent bacterial adhe-sins and lipopolysaccharide via the Toll-like receptorpathway resulting in neutrophil recruitment and inXuxinto the bladder lumen. Interactions mediated by type-1Wmbriae with the epithelium stimulate exfoliation of superWcial

epithelial cells, causing many of the pathogens to be shedinto the urine. Despite the inXammatory response and epi-thelial exfoliation, UPEC are able to maintain high titers inthe bladder for several days, and in chronic infections evenpersist for long period of times.

A bacterial mechanism of type-1 Wmbria-mediated inva-sion into the superWcial epithelial cells apparently allowsevasion of these innate defenses.

Recent studies in experimental models [6] [7], partlysupported by observations in human UTI [8], suggest thatbacteria initially replicate intracellularly as disorganizedclusters. Subsequently, bacteria in the clusters divide with-out much growth presumably due to changes in genetic pro-grams. Furthermore, the clusters become compact andorganized into bioWlm-like structures, termed intracellularbacterial communities (IBCs) [6]. Bacteria in the IBCs areheld together by exopolymeric matrices, reminiscent of bio-Wlm structures. At some point during this developmentalprocess of IBCs, bacteria on the edges of IBCs becomemotile again and start to move away from IBCs. Bacteriacan leave infected bladder cells, probably due to compro-mised membrane integrity. UPEC undergo such IBC cas-cade to increase in numbers, resulting in high bacterialtiters in the bladder. In addition, bacteria in these intracellu-lar niches can create a chronic quiescent reservoir, whichcan persist undetected for several months without bacteriashedding in the urine [7].

Pyelonephritis and bioWlm

Once bacteria reach the kidney, they are able to adhere tothe urothelium and papillae. It was shown in animal modelsthat bacteria could adhere in thin bioWlms to the urotheliumbefore invading the renal tissue (LeE 2b) [9]. Antimicrobialagents are more eVective against these bioWlms than againstthose on catheters [10], which may be due to the synergisticeVect of antimicrobial agents and host defenses [11].

Bacterial vaginosis

The vaginal Xora of healthy women consists predominantlyof Gram-positive lactobacilli. The vaginal microbiota ofwomen with bacterial vaginosis (BV) showed a loss of Lac-tobacillus species and an increase in microbial diversitydominated by Gardnerella vaginalis [12].

The recurrence nature of this disease prompted the spec-ulation that bacterial bioWlms are involved in BV. Swidsin-ski and co-workers demonstrated the presence of bacterialbioWlms on the vaginal epithelium of women with BV [13].Furthermore, in a subsequent publication, Swidsinski andcolleagues reported the resurgence of dense bacterial bio-Wlms at 1-week post-cessation of metronidazole treatment [14].These bioWlms were comprised principally of G. vaginalis and

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Atopobium vaginae. These data strongly support theinvolvement of bacterial bioWlm in BV.

BioWlm formation on foreign bodies in the urinary tract

Indwelling urethral catheters

Urinary catheters are targets of bioWlm development ontheir inner and outer surfaces once they are inserted (LoE2b). By the extraluminal route, organisms ascend the cathe-ter at the time of the catheter insertion. These organisms areprimarily endogenous, originating from the gastrointestinaltract. They colonize the patient’s perineum and ascend theurethra after catheter insertion.

Bacteria can ascend the catheter also by an intraluminalroute, which occurs when organisms gain access to theinternal lumen of the catheter. These organisms are usuallyintroduced from exogenous sources, for instance withcross-transmission from the hands of health care personnel.

The most frequently isolated strains from catheterizedpatients are Enterococcus faecalis, Pseudomonas aeruginosa,and Escherichia coli, while the strongest bioWlm producersare Proteus mirabilis, E. faecalis, Candida tropicalis, andStaphylococcus aureus. Strains with strong bioWlm formingability appear to be responsible for bioWlm formation inmixed-species bioWlms [15].

Ureteral stents

Bacterial bioWlm can also develop on ureteral stents that arelying completely within the urinary tract (LoE 2a). It hasbeen shown that while 68–90% of ureteral stents becomecolonized, the rate of bacteriuria in the same patients is only27–30% [16, 17]. These studies conWrmed the diYculty in

detecting bioWlm formation by using conventional labora-tory procedures. Therefore, a negative urine culture doesnot rule out the possibility of stent colonization.

The role of bioWlms in the encrustation of catheters

A frequent clinical problem with the use of medical bioma-terials in the urinary tract is the development of encrusta-tion. When the drained urinary tract becomes infected byurease-producing bacteria such as Proteus mirabilis, thebioWlms that form on the devices are especially problem-atic. The urease derived from Proteus mirabilis hydrolyzesurea six to ten times faster than the urease of other species.The ammonia generated by the urease elevates the pH ofthe urine. Under these alkaline conditions, hydroxyapatiteand struvite crystals are formed and trapped in the organicmatrix surrounding the cells. In the meantime, bacteria con-tinue to form bioWlm on the surfaces. Progression of theseencrustations eventually blocks the catheter lumen [18](Fig. 1).

BioWlm formation and incrustation also contribute to thelimited eYcacy of diVerent antimicrobial catheter coatings,because the deposition of crystalline layer to the catheterallows bacteria to attach and multiply without having con-tact with the underlying protective coating [19].

Infected urinary calculi

In case of urease-producing bacteriuria, the infection canbe conjoined with the formation of struvite and calciumphosphate calculi. The infected calculi grow rapidly andprovide safe environment for the bacteria adhered to thebioWlm (LoE, 3) [9]. The complete removal of all stonefragments, prolonged administration of antibiotics, andmetaphylaxis are the features of the most eVective treat-ment strategy.

Fig. 1 Scanning electron microscopic pictures of developed encrustations and bioWlms on stents, diVerent sections and enlargements

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ArtiWcial urinary sphincters (AUS)

Around 3% of the AUSs become infected. Avoiding therisk factors as infected urine, prolonged urinary retention,and large bladder residual can reduce this occurrence [20].Since the parts of the device form one continuous surface,the AUS is suggested to be removed entirely as the Wrst stepto eliminate the infection. The reimplantation must be pre-ceded by the complete treatment of the infected area [20].

Penile prostheses

Staphylococcus species, especially Staphylococcus epidermi-dis, are the most common pathogens found in penile prosthe-ses infection. The majority of prosthesis infections occursecondary to bacterial seeding at the time of surgery. Culturepositive bacteria were found in 70% of patients with clini-cally uninfected penile prostheses during revision surgery formechanical malfunction, with 90% growing Staphylococcusspecies [21], which have an enhanced ability to produceglycocalyx bioWlm. Because in most cases bacterial contami-nation occurs at the time of surgery, most common patho-genic organisms most likely to produce infections must betargeted when choosing prophylactic antibiotics.

To reduce the risk of device-associated infections, manymodiWcations have been developed. Hydrophilic penileprosthesis coating has been shown to decrease bacterialadherence in vitro and in animal models [22]. Further, thiscoating absorbs intraoperative antibiotics that can elute intosurrounding tissues to further decrease infection (LoE 2b).However, clinical data on the hydrophilic-coated penileprosthesis are limited.

The use of penile prosthesis coated with a combinationof rifampin and minocycline was approved in 2001. Theuse of these antibiotic-coated prostheses reduced the infec-tion rate with 58% compared to similar implants withoutthe coating [23].

Methods of prevention for bioWlm formation in the urinary tract

ModiWcation of the biomaterial surface

Since bioWlm formation has been realized as the main prob-lem of all implants and devices, modiWcation of the bioma-terial surface was regarded the most promising preventionstrategy for bacterial bioWlms.

Antibiotic-impregnated catheters

In a recent Cochrane Review, the authors found that antibi-otic-impregnated catheters signiWcantly lowered the rate of

asymptomatic bacteriuria (ABU) compared with uncoatedcatheters at less than one week of catheterization in case ofminocycline, rifampicin, and nitrofurazone (LoE 1a) [24].The diVerence was not statistically signiWcant at greater thanone week, and the authors concluded that the data were toofew to draw conclusions about long-term catheterization.

Silver alloy coating

According to the same Cochrane Review, silver alloy cath-eters signiWcantly reduced the incidence of ABU at lessthan one week of catheterization (LoE Ia) [24]. Beyond oneweek, the estimated eVect was smaller but the risk of ABUwas still less in the silver alloy group. There are no avail-able clinical trials with appropriate setting in case of long-term catheterization.

Hydrophilic coating

Hydrophilic-coated catheters are widely used in clean inter-mittent catheterization (CIC). In a prospective, comparativemulti-center study, the authors found that fewer patientsusing hydrophilic-coated catheter (64%) for CIC experi-enced UTIs compared to the uncoated catheter group(82%)[25].

However, in a recent randomized controlled study, theauthors did not Wnd signiWcant diVerence between hydro-philic-coated and uncoated urethral catheters in place for6 weeks with respect to symptomatic UTIs and microbio-logical analysis of urine culture [26].

Heparin

Heparin with its strong electronegativity that repels cellularorganisms is an excellent candidate for an anti-adhesivestent coating. In 1987, Ruggieri et al. showed a 90% reduc-tion of bacterial adhesion on catheters by heparin coating[27]. Heparin-coated ureteral stents did not show anyorganic or anorganic deposits after being in situ for up to6 weeks whereas signiWcant bioWlms were demonstrated in33% of uncoated stents [28].

On the other hand, Lange and co-workers tested heparin-coated, triclosan eluting and non-eluting control ureteralstents for adherence of common uropathogens for 7 days.Heparin coating did not decrease bacterial adherence com-pared with uncoated controls in this in vitro setting [29].

Gendine

Gendine is a novel antiseptic, containing Gentian Violetand chlorhexidine. Hachen and colleagues compared thein vitro anti-adherence activities of Gendine-coated uri-nary catheters and uncoated controls against several

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multidrug-resistant bacteria. Gendine-coated catheters reducedthe bioWlm adherence of all organisms compared withuncoated catheters. Scanning electron microscopy analysisshowed that a bioWlm layer overlaid the controls but not theGendine-coated catheters. The authors conWrmed theirresults in an in vivo rabbit model [30]. Although preliminarydata using this coating are promising, studies in the clinicalsetting are not available so far to validate its eYcacy.

Triclosan

Triclosan is an antibacterial compound that has been usedin consumer products for about 40 years. Triclosan elut-ing stent decreased the rate of UTIs and the bacterial loadin a rabbit model of cystitis caused by Proteus mirabilis[31]. In the study by Lange and co-workers cited above[29], triclosan eluting stent resisted all bacteria exceptPseudomonas and Enterococcus. Mature bioWlms wereobserved on all stents with lower viability on the triclosaneluting stent.

Use of low-energy surface acoustic waves (SAW)

The concept of using low-energy SAW is based on thehypothesis that these acoustic waves are able to disrupt theformation of bioWlms if transmitted directly to indwellingmedical devices by inhibiting the adhesion of planktonicbacteria to their surface. Hazan et al. devised an approachin which the acoustic waves spread from a portable actuatorgenerating piezoelectric vibrations at frequencies rangingfrom 100 to 300 kHz to the catheter surface [32].

They exposed SAW-treated and control catheters tostreaming Xuid containing diVerent uropathogens for3 days. SAW treatment reduced bioWlm formation, leav-ing catheters virtually clean of adherent microorganisms.They conWrmed their result in an in vivo animal model whererabbits where catheterized with SAW-treated and controlcatheters for 1 week. SAW-treated catheters showedstrong inhibition of bacterial bioWlm compared with thecontrols.

In a double-blind, sham-controlled randomized studyrelated to short-term catheterization, applying SAW releas-ing device to catheters prevented bioWlm formation in allthe catheters whereas bioWlm was present in 63% of thecontrol group [33].

A workgroup of the authors of the present article per-formed a prospective parallel group comparative study onthe eYcacy of the SAW treatment in case of long-termcatheterization (8 weeks). SAW treatment lowered the rateof signiWcant bacteriuria (33% vs. 81%), and the rate ofbioWlm formation was also lower in the SAW group com-pared with the controls [34].

Conclusion

With the increasing number of biomaterial devices used inurology, having an eVective method for preventing bioWlmformation is of utmost importance. Although the mecha-nism of bioWlm formation has been extensively researched,such ideal method has not been developed yet. SeveraldiVerent approaches are being investigated, and somepromising results have been obtained. The future goal is toidentify eVective mechanisms for the prevention and con-trol of bioWlm formation and to develop antimicrobialagents eVective against bacteria in bioWlms. Easier methodsfor diagnosing bioWlm infections have to be deWned.

ConXict of interest All co-authors have seen and agree with the con-tents of the manuscript, and there is no Wnancial interest to report.

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