Elsevier

Acta Biomaterialia

Volume 50, 1 March 2017, Pages 20-40
Acta Biomaterialia

Review article
A review of the recent advances in antimicrobial coatings for urinary catheters

https://doi.org/10.1016/j.actbio.2016.11.070Get rights and content

Abstract

More than 75% of hospital-acquired or nosocomial urinary tract infections are initiated by urinary catheters, which are used during the treatment of 15–25% of hospitalized patients. Among other purposes, urinary catheters are primarily used for draining urine after surgeries and for urinary incontinence. During catheter-associated urinary tract infections, bacteria travel up to the bladder and cause infection. A major cause of catheter-associated urinary tract infection is attributed to the use of non-ideal materials in the fabrication of urinary catheters. Such materials allow for the colonization of microorganisms, leading to bacteriuria and infection, depending on the severity of symptoms. The ideal urinary catheter is made out of materials that are biocompatible, antimicrobial, and antifouling. Although an abundance of research has been conducted over the last forty-five years on the subject, the ideal biomaterial, especially for long-term catheterization of more than a month, has yet to be developed. The aim of this review is to highlight the recent advances (over the past 10 years) in developing antimicrobial materials for urinary catheters and to outline future requirements and prospects that guide catheter materials selection and design.

Statement of Significance

This review article intends to provide an expansive insight into the various antimicrobial agents currently being researched for urinary catheter coatings. According to CDC, approximately 75% of urinary tract infections are caused by urinary catheters and 15–25% of hospitalized patients undergo catheterization. In addition to these alarming statistics, the increasing cost and health related complications associated with catheter associated UTIs make the research for antimicrobial urinary catheter coatings even more pertinent. This review provides a comprehensive summary of the history, the latest progress in development of the coatings and a brief conjecture on what the future entails for each of the antimicrobial agents discussed.

Introduction

Urinary catheters have been used since the third century B.C., by the Greeks, Egyptians and Chinese, but the first malleable urinary catheter on record was only made in 1779 by a goldsmith, Bernard [1]. Some of the first materials used to make urinary catheters were copper, tin, bronze, gold, lead, papyrus, onion stems, dried reeds and palm leaves. In recent times, materials such as gum-elastic, plastic (poly(vinylchloride), PVC), polyurethanes, silicone and latex rubbers have been used for their superior malleability [2], [3]. These materials have been developed over the years to include most of the characteristics desirable in a catheter: high tensile strength, soft and pliable, inherently chemical resistant, biocompatible and able to meet flow requirements while maintaining a minimally invasive circumference or French profile. Some of the strengths and weaknesses of different urinary catheter materials have been listed in Table 1, and these characteristics have led the emergence of silicone as the material of choice for urinary catheters despite a few of its disadvantages [1], [4], [5]. While latex was originally used alone, or modified with either hydrogel or Teflon coatings, its unsuitable properties like poor UV and chemical resistance, poor adherence, and possible allergic reactions leave much to be desired [1]. It has also been observed using scanning electron microscopy (SEM) that the rough surface of latex can also promote biofilm formation [6]. Therefore, silicone is now more commonly used as a base catheter material since it circumvents many of the problems faced by latex catheters.

Besides the evolution of materials, catheter design has also undergone several changes over the years including the balloon used to hold the catheter onto the urinary bladder and development of the modern indwelling catheter, also called the ‘Foley’ catheter, designed by Dr. Frederick B. Foley in mid 1930s [1]. This evolution of materials and design has been steered by the efficiency and comfort the catheter is able to provide to the patient along with availability of materials and technology. Currently, medical device companies like C. R. Bard, Inc. (Murray Hill, NJ), Coloplast (Minneapolis, MN) and Teleflex (Morrisville, NC) manufacture urinary catheters that contain advanced formulations with silver alloy (for example, gold and palladium) coatings and hydrogels that claim to dramatically reduce infection rates down by 3.7 times the standard urinary catheters.

Urinary catheters are used to manage urinary incontinence, urinary retention, and/or after prostrate or genital surgical procedures. In simple terms, urinary catheters are used to remove urine from the body. If the body is unable to remove urine for some reason, pressure builds on the urinary bladder and as a result, kidney failure can occur. Currently, there are several types of catheter designs that serve different purposes as shown in Fig. 1. The condom or single-use catheter is used for males who may have mental disabilities and have trouble urinating. These types of catheters are changed daily. The intermittent or short-term use catheter is used for a few weeks. This is commonly used for postoperative care when the patient is unable to urinate by themselves and need assistance. The long-term use or Foley catheters are typically used for several months at a time by patients with urine retention problems including those with spinal cord injury/disease, multiple sclerosis, enlarged prostate, or cerebrovascular accident. A management system/protocol for the insertion and removal of urinary catheters is maintained by different hospital systems. This includes the use of gloves, handwashing, sterile barrier, no-touch insertion techniques and training [7]. However, despite the care taken to avoid contamination and subsequent infections, catheters are still susceptible to accumulation of microbes. In urinary catheters, these microbes can accumulate to form single species biofilms, which can cover even short-term non-Foley catheters in a period as short as 24 h, which can ultimately develop multi-species biofilms causing infections if not detected at an early stage. Infection occurs in 10–50% of patients undergoing non-Foley or short-term urinary catheterization (7 days) but virtually all patients undergoing Foley or long-term catheterization (>28 days) become infected [8]. Foley catheters are most susceptible to infection as bacteria can collect and grow rapidly over time if not identified. This infection is called catheter-associated urinary tract infection (CAUTI), an infection that has stimulated antimicrobial materials research for urinary catheters.

Catheter-associated urinary tract infections account for over 1 million cases in the US alone [9] and almost 80% of the nosocomial infections worldwide [10]. Annual treatment costs exceed $350 million every year, which illustrate the urgency of the situation [10]. Some of the signs and symptoms of normal urinary tract infections (UTIs) and CAUTIs overlap, [11] as summarized in Table 2 of this review but the term CAUTI is assigned to patients who have been catheterized for over 24 h and show signs and symptoms of CAUTI within 48 h of catheterization. Urinary tract infection is defined as an invasion of any part of the urinary system by a bacterial or fungal pathogen [12], [13]. Nosocomial CAUTI is defined as the new appearance of bacteriuria or funguria in the urine at a concentration greater than 105 CFU mL−1 according to the Centers for Disease Control and Prevention. CAUTIs are caused by the invasion and colonization of pathogens through the route of the urinary catheter [14]. Such infections can cause mild to severe symptoms and pose a major cause for concern, as 15–25% of hospitalized patients use urinary catheters [14]. Catheter-associated urinary tract infection, when left untreated, may cause infections in the kidneys (pyelonephritis) and bloodstream (septicemia) [15], leading to sepsis or, in extreme cases, even death. The urinary catheter, a partially implanted device, can cause a patient to be highly prone to infections mostly because of cross contamination from the drainage bag and the rich microbial flora of the skin. This susceptibility increases with the duration of catheterization, which allows bacteria to flourish.

Long-term catheterization is needed when a patient suffers from urinary incontinence which entails inserting the catheter into the bladder for several months or years [1]. A major hindrance regarding the use of these long-term catheters is their ineffectiveness to prevent infection. Infections occur due to free-floating (planktonic) bacteria or encrustation of bacteria developing biofilms on catheter surfaces [16]. According to Dr. J. L. Brusch, an infectious disease specialist in Cambridge, Massachusetts, 90–100% patients who undergo long-term catheterization develop bacteriuria and 80% nosocomial UTIs are caused by catheters while only 5–10% are related to genitourinary operation [17]. For these reasons, the emergence of research in CAUTI and urinary catheters has been influenced by the enormous amount of health risks and healthcare-associated economic pressures caused by CAUTIs.

Two main issues that afflict urinary catheters and make it harder to treat CAUTIs are encrustation and biofilm formation [8]. While they are two different mechanisms caused by different factors, they can overlap and make conditions worse in an infection. Encrustation (Fig. 2) begins with the colonization of the catheter by urease-positive pathogens. Some urease-positive pathogens are P. mirabilis, M. morganii, P. aeruginosa, K. pneumoniae and P. vulgaris [18]. Urease is an enzyme that catalyzes the hydrolysis of urea into ammonia and carbamate. The presence of urine in urinary catheters creates a suitable environment for urease-positive pathogens. Ammonia is alkaline, and increases the pH of urine, leading to deposition of calcium and magnesium phosphate crystals on the catheter, which eventually leads to complete occlusion of the catheter through encrustation or crystalline biofilms [19]. One of the most common bacteria that causes encrustation is the urease-positive bacteria Proteus mirabilis [20]. P. mirabilis is a gram-negative, rod-shaped bacterium and causes 90% of all Proteus infections in humans and 20–45% of catheterization related infections [21]. In 1993, Stickler et al. presented a case study in which the patient’s catheter was completely blocked within 4–5 days of use [22]. The biofilms in the catheter contained elevated levels of mineral deposits. The ability of P. mirabilis to colonize all available types of indwelling catheters allows it to form secure biofilms in the catheterized tract and cause persistent catheter blockage. The infection can be diagnosed by an increase in the urine’s pH, fishy odor (produced by the bacteria) and P. mirabilis can be detected by its inability to metabolize lactose (on a MacConkey agar plate). A common treatment for Proteus infections is the use of antibiotics in urinary catheters, which can break down the biofilms formed by these persistent pathogens.

Biofilms are another major problem faced by urinary catheter patients because of the inherent property of urine to deposit minerals once infection by any microbe has occurred [18]. Free-floating, or planktonic, bacteria come across a surface submerged in the fluid and within minutes become attached. These attached bacteria produce slimy, extracellular polymeric substances (EPS) that colonize the surface (Fig. 3) and form the conditioning film. Extracellular polymeric substance production allows the emerging biofilm community to develop a complex, three-dimensional structure that is influenced by a variety of environmental factors. Biofilm communities develop within hours. Scanning electron microscopy and transmission electron microscopy have been used to document biofilms in urinary catheters removed from patients [23]. Biofilms have been reported to be approximately 200 μm in thickness and occasionally reach a thickness of ∼500 μm [24]. The rate of bacterial cell attachment depends on the number and types of bacteria in the urine or environment to which the catheter is exposed, the flow rate of liquid through the catheter, and the physicochemical characteristics of the surface of the catheter. It has been found that catheter surfaces that display both hydrophobic and hydrophilic properties attract the widest variety of CAUTI pathogens [25]. The bacteria can also propagate other biofilm communities by detaching in parts and attaching themselves elsewhere on the surface. A major hindrance in attacking and eliminating these biofilms is the extracellular polymeric substance that protects the cells, which allows the biofilm to exude high tolerance to stress from antibiotics and other biocidal treatments [26]. In fact, a biofilm’s tolerance to antibiotics has been attributed to three possible characteristics of the biofilm [27]: 1) slow penetration of antibiotics due to the matrix formed by the exopolysaccharides [28]; 2) formation of a resistant phenotype called persister cells that remain in a transient dormant state and can cause recurrent infections [29]; and 3) an altered environment within the biofilm that is composed of different anaerobic niches, concentration gradients and local accumulation of acids and inhibitive waste products. Hence, a major research development that has propagated the advancement in antimicrobial urinary catheter materials is the discovery of bacteria that cause CAUTIs by building single species biofilms and ultimately cause co-infection by forming multi-species biofilms (Table 3) [30], [31]. This has allowed researchers to develop mechanisms and bacteria specific or broad spectrum biocidal techniques to prevent CAUTIs. Some of the most common bacteria associated with CAUTIs are S. aureus, E. coli, P. aeruginosa. mirabilis, S. epidermidis, E. faecalis, and K. pneumoniae [8]. Several studies reveal that it is important to focus on the prevention of the biofilm rather than focus on planktonic bacteria as slow growth of the biofilms can confer resistance [32]. For example, in a rabbit catheter model study, only the highest dosage (400 mg/kg) of the antibiotic, amdinocillin could eradicate an E. coli biofilm formed on the catheter [33]. Another study showed how vancomycin concentration in an S. aureus biofilm was inversely related to the biofilm growth but it was also unable to completely eradicate the biofilm [34]. This meant that a biofilm’s resistance was related to the diminished effect of the antibiotic in the biofilm rather than poor penetration of the antibiotic. Another major hurdle in eradication of CAUTIs has been the increased incidence of infection due to polymicrobial infections, also called coinfection. As we know, single species biofilms can develop to form multi-species biofilms, studies to understand this effect on CAUTIs are important. One study found out that coinfection by P. mirabilis and P. stuartii caused an increase in the incidence of bacteremia and urolithiasis in a mouse model [35]. In fact, a detailed review on infection and coinfection by P. mirabilis has been published by Armbruster and Mobley [20]. This development in the body of knowledge of known pathogens of CAUTI has helped in understanding the mechanism of biofilm formation in specific bacteria, which aids in designing target specific biocides. While bacteria form the majority in the pool of pathogens, fungi are not far behind in CAUTIs. Ramage et al. have reported that C. albicans is frequently found in CAUTI biofilms and is the cause of 10–15% of cases [36]. Antifungal therapy and catheter removal have been described as the best therapies for treatment. A major drawback of studying and eliminating all pathogens associated with CAUTI is that a percentage of the pathogens in biofilms cannot be cultured by traditional microbial methods [37]. Even though they can be observed using microscopy, they cannot be cultured traditionally. Frank et al. devised a way to work around this problem using rRNA-based molecular phylogenetic methods to identify pathogens that form CAUTI biofilms [38]. This method did not require any culturing and relied on searching for the genomic sequences with BLASTN search and molecular-phylogenetic analysis. This study showed how further molecular studies could be conducted to find clinically-relevant microbes involved in CAUTIs across different regions of the world.

Despite all of the research effort that has gone into finding techniques and methods to solve the problem of infections caused by urinary catheters, most approaches have failed because of the rising problems associated with microbial resistance. It is also safe to assume that microbial studies alone will not eradicate CAUTIs, researchers need to understand the interaction of the microbes with the materials and their evolution as infection progresses.

Alexander Fleming’s serendipitous discovery of penicillin marked the beginning of the modern medical era of antibiotics and has likely saved more lives than most other medical advances in history. But as early as 1946, he also noted that, “There is probably no chemotherapeutic drug to which in suitable circumstances the bacteria cannot react by in some way acquiring ‘fastness’ (resistance)”. According to the WHO, antimicrobial resistance happens when microbes change upon exposure to antimicrobial drugs. This causes them to develop resistance and as a result, infections do not subside. Antibiotic resistance has led to the development of “superbugs” that are resistant to many antimicrobial therapies that in turn has compounded the problem of nosocomial infections.

The WHO has reported several instances of rising resistance among commonly found nosocomial pathogens [39]. Resistance to several antibiotics have been reported so far: carbapenem resistant K. pneumoniae, fluoroquinolone resistant E. coli, multidrug resistant S. aureus (MRSA) and colistin resistant Enterobacteriaceae. It is important to note that these bacteria are also commonly found in CAUTIs, and hence their infection raises issues of resistance to the antimicrobial agents used in urinary catheter materials.

A long-term study was conducted by Wazait et al. between 1996 to 2001 in the UK to collect information on catheter urine samples to identify change in bacterial profile and antibiotic resistance in CAUTI [40]. The samples were collected in 1996, 1998 and 2001. E. coli and Enterococcus were the most common pathogens. Frequencies were 35.6%, 32.5% and 26.6% for E. coli and 11.8%, 15.3% and 22.0% for Enterococcus for 1996, 1998 and 2001. The results also indicated a change in pattern of antibiotic resistance along with this change in frequency of the bacteria profile. In 1996, bacteria were least resistant to ciprofloxacin (8.0%), co-amoxiclav (18.5%) and cephalexin (25.4%) but in 2001 the resistance changed to co-amoxiclav (22.5%), ciprofloxacin (27.2%) and nitrofurantoin (28.8%). As of now eight pathogen groups that make up 80% of antimicrobial resistant bacteria found in nosocomial infections are MRSA (8.5%); vancomycin resistant Enterococcus (3%); extended spectrum cephalosporin-resistant K. pneumoniae and K. oxytoca (2%), E. coli (2%) and Enterobacter spp. (2%); carbapenem resistant P. aeruginosa, K. pneumoniae and K. oxytoca (<1%), E. coli (<1%) and Enterobacter spp. (<1%) [41]. Studies like the two highlighted above should be performed in other regions of the world to identify and appropriately detect any change in the resistance profile for CAUTI pathogens. This would aid and supplement microbial studies along with the development of antimicrobial coatings that can attack even multidrug resistant CAUTI pathogens.

Various approaches can help to prevent CAUTI, such as better handling of catheters, fabricating urinary catheter coatings, improving catheter design, and emphasizing short-term use. However, this review focuses on urinary catheter coating materials designed to prevent CAUTI either by their antifouling or biocidal properties, or both. While the other approaches can help in preventing CAUTI, sometimes patient comfort in case of design and need for long-term use can hinder the utilization of these approaches. In contrast, fabricating biocidal and antifouling materials is a simpler task as long as the materials do not pose side effects like development of antimicrobial resistance and patient allergy. As healthcare-associated costs have risen over the past two decades and population around the world has increased, the need for better catheter materials has substantially increased. Hence, research on antifouling and biocidal materials for catheters has centered on designing the most competent, yet simple, material in terms of use and fabrication. Although the sophisticated antimicrobial coatings for urinary catheters may cost more than the standard urinary catheters, they make up for this cost in the long run by preventing nosocomial infections, the treatment of which is generally not covered by most insurance policies.

Antifouling coatings do not kill the microbes directly but instead prevent the attachment of bacteria on the surfaces that allow the formation of biofilms [42], [43]. Mechanisms of antifouling materials include steric repulsion, electrostatic repulsion and low surface energy (Fig. 4 A, B and C) to keep foulants from attaching to the surface of the catheter. This prevents the formation of conditioning films for planktonic bacteria that ultimately form biofilms, the stage at which is hardest to treat with antimicrobial agents. Generally, materials that are antifouling by the mechanism of steric repulsion are bioinert in nature [44], [45]. This means that they tend to avoid any interaction with their surrounding environment. The two main types of antifouling materials currently in research are made of hydrophilic materials (e.g. SAM-OEG, PEG, POEGMA) [46], [47], [48] and polyzwitterions (e.g. polyMPC, polyCBMA, polySBMA) [49], [50], [51]. They repel foulants by forming a barrier of hydration layer on the surface [52], [53]. This hydration layer is formed through hydrogen bonding and/or ionic solvation. When the proteins approach the surface, water molecules are released from the surface and the polymer is compressed. This leads to an increase in enthalpy due to polymer dehydration and decrease in entropy due to chain compression. According to thermodynamics, both of these events are unfavorable and hence these surfaces tend to repel proteins or other foulants by the mechanism of steric repulsion [44], [46].

On the other hand, biocidal urinary catheter materials are designed to kill the microbes instead of minimizing their deposition. These catheters are essential because they protect the patients from infection and encrustation development. Several biocidal materials have been developed to combat the problem of CAUTIs and decrease associated hospital care costs. Clinically tested biocidal coatings have silver or antibiotics as the active ingredient. While these agents are predominant in the clinical field, many other agents (triclosan, chlorhexidine, nitric oxide, enzymes, peptides) or agent carriers (liposomes, polymers) are currently in the research stage, and will be discussed in the next section. The most common mechanisms for biocidal actions fall into 5 basic categories according to their mechanism of action: 1) Inhibition of cell wall synthesis (e.g. chlorhexidine, penicillin and vancomycin) 2) Inhibition of protein synthesis (e.g. silver ions, nitric oxide and tetracyclines like minocycline) 3) Inhibition of nucleic acid synthesis (e.g. sparfloxacin, quinolones, nitric oxide and rifampin) 4) Effects on cell membrane sterols (e.g. silver ions, triclosan, antimicrobial peptides and antifungal agents like amphotericin B) 5) Inhibition of unique metabolic steps (e.g. nitrofuran, triclosan, bacteriophages and sulfonamide). Cell walls are not present in humans and mammals but are an important component in bacteria. Biocides can inhibit the formation of peptidoglycan and dephosphorylation of phospholipid carrier in peptidoglycans, which ultimately leads to death of the microbe. For inhibition of protein synthesis, biocides attack by attaching themselves to the ribosomal subunits (50 s and 30 s) in bacteria. Proteins are necessary for multiplication and survival in bacteria and thus their disruption causes cell death. Nucleic acids are the key for replication. When biocides inhibit mRNA synthesis, DNA gyrase, topoisomerases and nucleic acid synthesis, they can kill bacteria. Cell membrane sterols are altered by some biocides but since cell membranes are present in both mammalian and bacterial cells, these biocides can also cause cytotoxicity. For this reason, these materials a typically used as the final line of defense against bacteria. Alteration of cell metabolism by inhibiting the synthesis of cofactors for nucleic acid synthesis and mycolic acid synthesis can also cause bacteria death by biocides. These biocidal agents can either be embedded in the polymer and be released to kill bacteria (Fig. 4 D) or they can be covalently bonded or crosslinked to the surface of the materials to kill microbes on contact (Fig. 4 E). Examples of agents which are mostly used in biocide release antimicrobial coatings are silver ions, triclosan, chlorhexidine, chlorine, tributyltin, nitric oxide, and antibiotics [54]. A commonly studied example of contact active biocidal agent is quaternary ammonium compounds [55], [56]. It is important to note here that some of the biocidal mechanisms of different agents can overlap (e.g. silver ions and antibiotics have two mechanisms in common) since these agents are categorized according to their structure and not mechanism of killing and some agents employ more than one mechanism of killing (e.g. silver, nitric oxide). In case of biocidal coatings that release biocides, the materials leach out their antimicrobial agent and hence do not let the microbe come in contact with the catheter. This can aid in preventing encrustation and biofilm formation. However, leaching of the biocide can also prove to be harmful, as we discuss later in the case of triclosan.

Antimicrobial and antifouling materials are the focal point of research in catheter materials, as they offer the potential for complete protection against CAUTIs [57]. These materials are proven to be efficient in preventing CAUTIs as they have a higher microbial cytotoxic ability [58]. However, it is also important to note that because of the high resistance of biofilms to antimicrobial agents, catheters that elute biocides to prevent contact of contact with urinary catheter would increase the efficiency of the coatings compared to contact active methods [59], [60]. This elution should be from both inner and outer surface of the catheters.

Although the problem of CAUTIs is complex and still a major challenge, materials that combine known and novel antimicrobial agents with an increase in effectiveness have shown tremendous progress. Examples include the use of silver alloy, a commonly used antimicrobial material, modified with plasma and silver nitrate and the use of antibiotics like rifampin and sparfloxacin in combination with antiseptics such as triclosan to increase the agent’s antimicrobial efficacy. While the list of antimicrobial agents along with new formulations continues to expand to combat the problem of CAUTIs, some of the more commonly studied urinary catheter coating materials (both in clinical trial and/or research) are highlighted in this article, along with a discussion of future research directions. In this review, the antimicrobial agents/materials for urinary catheters have been categorized broadly into two categories: Clinically tested antimicrobial catheter agents/materials and researched (but not clinically tested) antimicrobial catheter agents/materials. Since it would be complicated to present them in smaller, sub-categories organized by their antifouling and biocidal mechanisms, we have categorized them into antimicrobial agents/materials and carriers of antimicrobial agents. The materials described herein are not an exhaustive list of the antimicrobial coatings that have been developed to date, but rather highlights of the major agent/material categories.

Section snippets

Silver

Silver is one of the few antimicrobial agents for urinary catheter coatings (along with other medical devices) that is approved by the FDA. Even low concentrations of Ag ions are enough to kill microbes. Its mechanisms for killing bacteria include 1) impaired membrane function by loss of membrane potential, 2) protein dysfunction by destruction of Fe-S cluster, and 3) oxidative stress by antioxidant depletion [61], [62], [63], [64], [65] (Fig. 5). The multifunctional mechanism of antimicrobial

Future perspectives and challenges

Currently, research on antimicrobial agents/materials for urinary catheters is aggressive and a direct result of the need to find viable solutions to CAUTIs. The interest in agents such as NO and antimicrobial enzymes also suggests that research will not slowdown in this area in the near future. For this reason, there are a couple of challenges that researchers need to focus on whether they are improving formulations with clinically tested materials or diving into ‘new research’ with urinary

Conclusion

CAUTI is one of the leading nosocomial infections in the world and has led to the study of various novel ways to prevent the infection. This has made “antimicrobial agents/materials for urinary catheters” a widely studied subject. Studies such as synthesizing novel gendine for antimicrobial gloves [195] could aid in preventing infections in the hospital settings. However, even after meticulous care and insertion of the catheters in sterilized conditions, infections still occur. This shows that

Acknowledgement

The authors acknowledge the support from the National Institutes of Health – United States, Grant K25HL111213.

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