bacterial biofilms on devices used in nephrology

Nephrology 1995; 1, 269-275

Review Article

Bacterial biofilms on devices used in nephrology GREGOR REID,lJ CHRISTINA TIESZER.1,3 AND Ross R BAILEY4

'Department of Microbiology and Immunology, 2Diwision of Urology, Department of Surgery, 3Department of Chemistry, The University of Western Ontario, London, Ontario, Canada and 4Department of Nephrology, Christchurch Hospitul, Christchurch, New Zealand

Summary: Prosthetic devices are commonly used in nephrological and urological practice for the management of urinary and peritoneal dialysis flow, haemodialysis and drainage of renal calculi after laser or lithotripsy treatment. Many different types of materials are used and a number of complications arise, yet the fundamental interactions which occur at these biomaterial surfaces have been little studied. Recent information has shown that host conditioning films are deposited onto materials upon implantation, and that dense bacterial biofilms can form and resist conventional therapy. In order to better manage patients with prostheses, it will be imperative to understand the processes arising in the host and, using scientific data, to select the optimal interventions.

Key words: bacterial biofilms, devices, nephrology, urinary.

INTRODUCTION

The use of biomaterials for medical applications has been increasing steadily with growth around 7% per annum and a global market for devices valued at $86 billion per year. A large proportion of the market comprises products designed to drain urine (catheters, stents, incontinence pads). * In relation to nephrology, there are many devices used, including Tenckhoff catheters, vascular catheters, drains and lines. Ureteral stents are devices which are designed to be self-retained within the ureter to drain urine from the renal pelvis to the bladder. If urine flow is obstructed, for example by encrustation of the lumen of the stent, renal damage may occur, particularly if infection is present.2 In the latter case, failure to eradicate the organisms quickly may result in severe sepsis.

Infectious complications arise at the exit site and in the peritoneum of peritoneal dialysis pa t ien t~ ,~ and femoral and subclavian central venous catheters become infected and obstructed.4 Biofilms have been found on many surfaces, including intravascular cathet- e r ~ , ~ urine droppers and collecting systems6 Immuno- compromised peritoneal dialysis patients are especially susceptible to systemic fungal infection^.^ The ability of

Correspondence: Gregor Reid, Research Services, SLB 328, The University of Western Ontario, London, Ontario N6A 5B8, Canada.

Received 20 June 1995; accepted 22 June 1995.

yeasts to burrow into materials and form dense biofilms has recently been shown8 Even after transplantation, infectious complications can occur and can be s e r i o ~ s . ~ Therefore, the stages which occur in the development of infections associated with devices such as stents, catheters and lines must be better understood if effective management is to be implemented.

CONDITIONING FILM AND ENCRUSTATION DEPOSITION ONTO BIOMATERIALS

Upon insertion, a biomaterial immediately comes into contact with body fluids such as urine and blood, and components of these adsorb onto the material depend- ing upon its surface properties. The existence of macro- molecular conditioning films which modify surfaces prior to microbial colonization and biofilm formation has been recognized for over 50 years.'O However, its importance in relation to the urinary tract is only now being appreciated.

When associated with cells and materials in the urinary tract, the nature of the substratum can play an important role in bacterial deposition. This generally non-porous surface is where the base conditioning film is deposited. The nature of the film appears to be influenced by the composition of the substratum, and both factors affect the bacterial attachment levels to the surfaces.

A crucial property of biomaterials is their biocompa- tibility, defined loosely as a property whereby a material

270 G Reid et al.

does not induce an acute or chronic inflammatory response or prevent proper differentiation of tissues which surround an implant.’l In a scenario known as the ‘race for the surface’, if cells cover a surface before bacteria (this really only applies to implanted, closed devices), then infection will be unlikely.12

BACTERIAL BIOFILM FORMATION

A biofilm has been defined as consisting of cells immobilized at a solid surface and frequently embedded in an organic polymer matrix of microbial origin.13 However, more recent scientific data indicate that the substratum can include human cells and t iSSue~,~4~~~ and that biofilms can also form at distances away from a substratum. 16-18 Although the term biofilm generally refers to multiple layers of organisms encased in a glycocalyx, it should be stated that, by definition, they can consist of less than a monolayer of cells or can be as dense as 400 mm. Typically, the biofilm will consist of a mini-environment where more than one species exists.

The ability of micro-organisms to form biofilms is widespread, including ship hull fouling, heat and water exchangers, dental plaque, gastroenteritis, fermentation systems, metal corrosion, submarine periscopes and air conditioning outlets, water cooling towers, oil pipes and many other systems. In essence, biofilms are composed of microbial cells and their by-products in a generally porous structure which contains as much as 95% water, along with solutes, inorganic particles and organic matter used by the organisms as nutrients.

The first stage in biofilm formation occurs with the conditioning film deposition. This is followed by bacteria approaching the surface, overcoming possible charge and hydrophobic barriers, then attaching and producing extracellular polymers. 19-21 Thereafter, the organisms grow at the interface and develop biofilms. A network of channels can be found connecting the various layers of the biofilm and allowing gas and nutri- ent exchange.18

Bacterial-associated encrustations are quite common in the urinary tract and invariably comprise struvite (MgNHQ0+6H20) or carbonate apatite (Cal0(PO4)C0,).22J3. In uitro models have been estab- lished and analysis by scanning electron microscopy (SEM) and energy dispersive X-ray analysis (EDX) has shown the presence of these Problems such as blockage of urinary flow can arise when encrustations deposit onto stents. If the deposits are associated with bacterial colonization, urinary tract infection (UTI) and bacteraemia can occur, and these can be difficult to eradicate unless the infected device and encrustations are removed.

IMPORTANCE OF BIOFILMS IN HEALTH WITH EMPHASIS ON THE URINARY TRACT

The presence of bacterial biofilms in the human body is widespread.8 As will be mentioned later, not all biofilms confer symptoms and signs of disease. In the urinary tract, pathogenic microflora can overgrow normal biofilms and form an infected state for many reasons, including a consequence of antibiotic therapy or sperm- icide use which disrupts the normal flora.z5-26

Biofilms have been found extensively in association with indwelling prostheses and open system device^.^'-^^

Physical and chemical properties of biofilms

The transfer of particles is much slower in laminar flow systems than in turbulent flow. This can alter the microbial activity within the system. Urine acts as the bulk liquid compartment which transports nutrients (and antibiotics) to the biofilm and carries away detached cells and products of metabolism. Within the biofilm, molecules diffuse from the bulk liquid to surface and base films. Daughter cells are believed to push components up through the film and into the liquid compartment. For example, as Proteus species are extremely motile, it is likely that their daughter cells would be able to move out to the bulk liquid compartment.

The biofilm, as an organic polymeric gel containing living organisms, has highly hydrated capsular material or viscous, soluble slime protruding from the bacteria and attached to the sub~tratum.~~ The macroscopic properties of the biofilm and the deposited encrustations which may be on a ureteric stent affect the rheology and morphology of the surface, and therefore the fluid friction and urine flow. The physical, chemical and biological properties present within a system (kidney, ureter, bladder, urine, material type) influence the biofilm which develops. The urethra is ofren the source of bacteria which colonize stents and generally few species of bacteria are found as biofilms on these devices. Once attached, the organisms modify their microenvironment and produce metabolic end- products which can adversely affect the host (e.g. haemolysin, lipopolysaccharide, toxins, immune stimu- lators, carcinogens). By deduction, it can also be presumed that the content of the urine itself has the potential to influence the biofilm micro-environment to a large degree. The question is how can this be utilized to the advantage of the clinician?

At the early stages of biofilm formation (adhesion in the secondary minimum), l2 physico-chemical properties of the bacterial surface, especially charge and hydrophobicity, dictate an organism’s ability to adhere to a

Bacterial biofilms in nephrology 27 1

given surface. After secondary minimum adhesion, specific adhesins, such as uropathogenic Escherichia coli type 1, lC, P, S and G fimbriae, and M, Dr and X, mediate binding as long as receptor sites are p re~en t . j ' -~~ The possession of certain 0 serogroups, 2, 4, 6, 8, 18ab and 75, high K-antigen titre, and production of haemolysin are also important contribu- tors to pathogenesi~.~~ In relation to biomaterial associated infections, it appears that the production of extracellular polymeric substances, invariably polysaccharides, leads to irreversible adhesion, and is responsible for biofilm integrity.39 These bacterial polysaccharides are divided into specific and non- specific classes.@ Common sugars, such as mannose, glucose, rhamnose, galactose, N-acetylglucosamine, glucuronic acid and galacturonic acid are typical of the former class. Lipopolysaccharides and teichoic acids, components of the cell membrane and wall of Gram- positive and Gram-negative organisms, respectively, are not defined as specific polysaccharides, but they share a common property of being antigenic.+'

Non-specific polysaccharides include extracellular cellulose, dextrans, fructans and alginate, the latter being produced by uropathogenic Pseudomonas aerugi- nosd2 and being shown to be important in colonization of catheters+) and epithelial ~ells.4~ Polysaccharides are important for many reasons,8 including energy storage (intracellular polysaccharides), reversible adhesion (cell surface bound), protection from host defences (matrix polymers) and microbial detachment (released polymers).

Thermodynamic modelling predicts that hydrophilic bacteria would adhere better to hydrophilic substrata and that hydrophobic organisms would adhere better to hydrophobic substrata but, in practise, it is not that simple."+-49 For example, E. coli expressing quite different surface adhesins have been found to have an overall hydrophilic surface property (Reid et al. unpubl. obs.), yet they attach to hydrophilic and hydrophobic rnate1-ials.4~ One possible explanation is that hydrophobic domains exist on proteins or as methylated polysaccharides on the bacterial surface or fimbriae, and these mediate adhesion to the hydrophobic substrata.

Various methods can be used to examine elemental composition of substances at the surface of biomaterials, as mentioned in the previous section on conditioning film deposition. Such studies have shown that carbon to nitrogen ratios can be higher in biofilms compared to bacterial cells alone, reflecting the extracellular matrix. Inorganic elements such as calcium can increase intermolecular bonding.51

Influence of solutions

The form and structure of the biofilm is influenced by

the composition of the suspending fluid, namely urine in the case of stents, catheters and drainage tubes, and peritoneal dialysate in the case of Tenckhoff cathet- e r ~ . ~ ~ Changes in pH, osmolality, temperature, organic salts and polysaccharides induce conformational transitions leading to, for example, increased stability of the biofilm. If uronic acids or pyruvate or other charged groups are present in the bacterial matrix or the bulk fluid, this can also influence the biofilm structure. For example, the matrix solubility is generally greater for charged polymers in polar solvents such as water. As urinary surface tension has been found to vary amongst people and between specimens,48 it is easy to hypoth- esize how alterations in the biofilms can occur. At low pH, acidic polymers within the glycocalyx are neutral- ized and may precipitate. Precipitation with cations such as calcium also occurs, which may in part explain why bacteria are often associated with crystalline structures on stents. The addition .of salts reduces viscosity of charged polysaccharides, causing contraction of extended stiff forms into smaller, more flexible structures. In the presence of water molecules, the biofilm develops a three-dimensional gel network. The effects of urea, creatinine and Tamm Horsfall glycoprotein on biofilm formation remain to be investigated; however, it has been shown that these constituents can influence bacterial a d h e ~ i o n . 4 ~ ~ ~ ~ ~ ~ 4

Bacterial metabolism within biofilms

Given that bacteria within biofilms are in close proxim- ity to each other, factors such as antagonistic and antibacterial by-products, competition for space and nutrients and synergy play a role in metabolic activity. In addition, the environmental and physico-chemical conditions (flow or stasis, electrolyte concentration, oxygen tension, availability of immobilized proteins and carbohydrates etc.) affect the attached mi~rocolonies.~~ The highly hydrated polymeric matrix can act as a gel diffusion barrier for nutrients.56 Within the biofilm, different bacterial species can be spacially separated or integrated, exchanging metabolites and genetic information including, potentially, drug resistance properties.57-58

The outcome can increase or decrease growth rates and no general phenomenon can be stated to occur. Studies on thin biofilms of less than 40 pm have shown that all bacteria are not fully active.59 Relatively inactive bacteria have been found in biofilms,60 and clinically these have been discovered in association with chronic bacterial prostatitis. In the latter case, it is believed that the metabolic rate is reduced upon exposure to antibiotics, then the rate increases once the therapy has stopped, thus explaining why the same infecting strain can cause a relapse.15

272 G Reid et al.

RESISTANCE TO ANTIMICROBIAL AGENTS AND POSSIBLE REMEDIES

The finding that bacteria within biofilms are less susceptible to antimicrobial treatment is a major clinical concern. Several studies have demonstrated this

It is believed that the polymeric matrix can restrict antibiotic penetration and that the organisms can lower metabolic rates to resist killing. Changes in porins, penicillin-binding proteins, and reduction in membrane phospholipids provide examples of how bacteria can react to antibiotic pre~ence.~5-67

The extent to which bacterial biofilms can resist antimicrobial action is well demonstrated in ureteral stents inserted into patients for days to week^.^^^^^ On occasion we have found dense bacterial biofilms embedded within encrustation material, and these organisms not only resist daily oral trimethoprim treatment, but also fail to be removed by severe sonication of the stent (Figs 1, 2).

There is some recent evidence that fluoroquinolones, especially ciprofloxacin and ofloxacin, can kill bacteria in the biofilm mode. Exposure of pathogens to ciprofloxacin, even at sub-inhibitory concentrations, can alter cell surface properties and elemental compo- s i t i o n ~ . ~ ~ Reduction in biofilm viability has been reported using in uitro experiments applied to material^^^,^^ and ~el ls .7~ Fourier transform infrared spectroscopy showed that the presence of a bacterial biofilm created an antibiotic diffusion barrier, resulting in a 17 min lag in the time required to establish bulk- phase drug equilibrium concentrations at the surface (Mittelman et al. unpubl. obs.).

Other studies have shown that a mixture of antiseptics can be effective at eliminating biofilms,74 and that protamine at concentrations of 100 pg/mL can signifi- cantly eradicate bacteria adherent to urinary ~e l l s .7~

Prior to awaiting the introduction of new materials or combination agents which kill biofilms, a study was carried out to determine whether antibiotics given orally could diffuse out of body fluids onto stents and thereby prevent and treat infection. The results show that oral administration of ciprofloxacin, a highly potent broad-spectrum fluoroquinolone antibiotic which penetrates bacterial cell walls and inhibits DNA gyrase activity, leads to adsorption of the drug from the urine onto stents. Of 30 patients studied to date no viable bacteria have been recovered from the urine or stents (Tieszer et al. unpubl. obs.). These results support the findings from a clinical study which showed that ciprofloxacin given prophylactically was a safe and effective way to prevent catheter-associated infections.76

Several research groups are currently studying the chemical bonding of antibiotics onto materials as a

Fig. 1 Scanning electron micrograph showing Gram- negative rods in biofilm mode (beside large round blood cells) associated with encrustations on a SofFlex ureteral stent. The female patient, treated for renal calculi by extracorporeal shock wave lithotripsy, had received daily trimethoprim for 10 days since insertion of the device, and no organisms were recovered from the urine. Bar = 2.73 pm.

Fig. 2 Scanning electron micrograph showing Gram-positive cocci in biofilm mode embedded in encrustations deposited onto a Sofflex ureteral stent. The male patient, treated for renal calculi by extracorporeal shock wave lithotripsy, had received daily trimethoprim for 26 days post-insertion, and no organisms were recovered from the urine. The glycocalyx material is seen linking the bacterial cells. Bar = 6.00 pm.

means to deliver drugs and prevent infection. The important chemical considerations will be to achieve a sufficient amount of drug bound to the surface to kill bacteria, yet to have low toxicity to the host, and to achieve a leaching rate of drug sufficient for several days or weeks of protection from infection. This type of research has been spawned by non-medical studies such as those which showed that removal of microfouling biofilms from the hull of a frigate increased its shaft- horsepower by 18O/0.~~ Therefore, the technology to

Bacterial biofilms in nephrology 273

reduce or eradicate biofilms has a broad applicability. The Low Surface Energy (LSE) stent (made by ion implantation and found to be relatively hydrophilic) and Sof-Flex Aqua (hydrophilic) stent, both produced by Cook Urological (New Zealand) may resist bacterial deposition to some degree. Preliminary studies with the LSE have indicated its potential to resist encrustation depo~i t ion .~~

Povidone-iodine is often used in nephrological and urological practice as an antibacterial agent. A recent study has shown that resistance to this agent appeared to be due to a protective layer of cells within the glycocalyx of P. aeruginosa, which increased the time required to detach the cells and expose them to the i0dine.7~

It will be important to develop tests which can quantitate biofilm responses to therapeutic agents, and a method using 2,3,5-triphenyltetraolium chloride has been developed, though not yet made widely avail- abie.79

APPARENTLY NON-INFECTIOUS BIOFILMS

In nature, biofilms serve as a sink for many toxic and hazardous materials and chemicals. Many examples can be given of research which is concentrating on the utilization of bacteria to degrade toxic compounds. To date, the nature of the urinary components that bacteria adherent to stents can extract from the urine is unknown. Clearly, certain urease-producing bacteria are able to extract calcium, phosphorus and magnesium from urine, which leads to infected struvite calculi.

In the urogenital tract, there are two examples where biofilms have been found, without onset of infection: the presence of Lactobacillus on intrauterine devices,a0 and the existence of potentially pathogenic biofilms on peritoneal dialysis cathetemal The reasons for these findings remain to be fully elucidated, but the obser- vation does support further investigation into whether or not non-infecting biofilms can be created to prevent infection.

CONCLUSIONS

For nephrology, as well as for other specialties, the future will see an increased application of biomaterials for the treatment of disease. Of more serious impact will be the inability of antibiotics to prevent and treat infections associated with such materials. A recognition of the presence of bacterial biofilms and the development of detection systems and eradication and preventive interventions will be crucial for patient care.

ACKNOWLEDGEMENTS

This work was funded by the Medical Research Council of Canada, Bayer Canada and the University Research Incentive Fund of Ontario. The assistance of Cook Urological and the PMAC Student Award is also acknowledged, as is the help provided by Surface Science Western.

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