Applications of Polymeric Materials with Antibacterial Properties

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This entry is adapted from the peer-reviewed paper 10.3390/ma16124411

The presence of antibiotic-resistant bacteria in people's environment is a matter of growing concern. The issue of multidrug-resistant bacteria urged the need to elaborate the novel antipathogen agents. The polymers and copolymers modified with bioactive compounds have emerged as a group of highly effective antimicrobial agents that find usage in many fields. The natural polymers have a great advantage over the synthetic ones due to their non-toxicity, biocompatibility, non-immunogenicity, and high stability. On the other hand, they are less effective in biomedical applications in comparison to synthetic polymers. The modifications that provide the natural polymers with desirable industrial activity include chemical treatment processes such as hydroxylation, carboxylation and epoxidation, or in vitro enzyme treatment.

polymeric materials antibacterial activity antibiotic-resistant bacteria

1. Antibiotic Resistant Bacteria in Environment

In recent years, the growing amount of antibiotics in wastewaters constitute a great challenge to the wastewater treatment plants, as the conventional methods—e.g., flocculation, sedimentation, filtration, or coagulation—are not sufficient to remove these pollutants from environment sewage ^[1]. The most abundant antibiotics found in sewage are trimethoprim, sulfonamides (SA), quinolones, and macrolides, the frequent occurrence of which results from their stability and wide application in the treatment of bacterial diseases in humans and animals ^[2].

Trimethoprim (TMP) is an antibiotic; its moieties contain electron-rich aromatic rings and a deprotonated amine group, and it is susceptible to the oxidation process, which is proposed as one of the ways to eliminate this compound from aqueous systems ^[3].

SA are a class of antibiotics that include sulfadiazine, sulfamethazine, and sulfamethoxazole (SMX). One of the possible pathways for the removal of SA is bioaugmentation, which leads to anaerobic degradation of these antibiotics ^[4].

Quinolones (ofloxacin, ciprofloxacin, norfloxacin) and macrolides (clarithromycin, erythromycin, azithromycin) were recorded in Asia and Europe with occurrence frequencies between 6–30% and 6–10%, respectively ^[5].

The widespread use of antibiotics contributes significantly to the resistance of bacteria to their bactericidal properties, which is a great challenge for modern medicine ^[6]. An excessive amount of prescribed antibiotics and their limited metabolism in human cells (30–90% of consumed antibiotics are not metabolized in the human body and are excreted into wastewater systems) leads to antibiotic exposure and accelerates resistance in bacteria ^[7]. The scheme of antibiotic distribution in the natural environment is presented in Figure 1.

Figure 1. Antibiotic distribution in environment.

Antibiotic resistant bacteria (ARB) acquire resistivity by producing antibiotic resistance genes (ARGs) through the cellular expression process ^[8]. The capacity of the horizontal transmission of genes in aquatic environments provides an easiness in the spread of antibiotic resistance among humans and animals, which poses a significant risk to health ^[9]. Antibiotics may enter the environment in the form of metabolites with the retained activity of the original drugs, or they may be excreted from the human/animal body as more polar derivatives of the original antibiotic, which can be then converted by the bacteria into the original drug ^[10]. ARBs are divided into multidrug-resistant (MDR), extensively-drug resistant (XDR) and pan-drug-resistant (PDR) bacteria, and the criterion for this classification is the number of classes of antibiotics to which the bacteria are resistant. MDRs are bacteria that are resistant to at least one drug belonging to three or more classes of antibiotics at the same time, XDRs are bacteria resistant to at least one antibiotic of each class, except for two or less antimicrobial categories, and finally, PDRs are bacteria resistant to all antibiotics in all antimicrobial categories. MDRs, which have become resistant due to high-volume and long-term use of antibiotics, are of particular concern in Chinese and European intensive care units, where they were responsible for 1.27 million deaths in 2019 ^[11]. Due to the ability of PDR to effectively withstand all forms of antibiotic therapy, test bacteria pose a particular threat to health facilities. Among the PDR, Gram-negative bacteria can be distinguished, i.e., E. coli, P. aeruginosa, K. pneumoniae, and A. baumannii. P. aeruginosa is the bacterium responsible for pneumonia, which is particularly common in intensive care units, and poses a particular threat to people suffering from cystic fibrosis and the formation of biofilms. Most nosocomial infections are caused by K. pneumoniae, also called the super bacteria, because it has become resistant to all the beta-lactams that make it difficult to treat diseases caused by this bacterium. Some E. coli strains may affect the urinary tract, digestive tract, spinal cord, and brain. A. baumannii can lead to pneumonia and infections of wounds and the intra-abdomen ^[12]. Carbapenem-antibiotics-resistant XDR bacteria such as P. aeruginosa, K. pneumoniae, and A. baumannii cause bloodstream infections with high mortality ^[13].

2. Polymeric Materials with Antibacterial Properties—Mechanism of Action and Medical Applications

It is predicted that antibiotic-resistant bacteria can result in 10 million deaths by 2050 ^[14]. The issue of multidrug-resistant bacteria urged the need to elaborate the novel antipathogen agents ^[15]. The polymers and copolymers modified with bioactive compounds have emerged as a group of highly effective antimicrobial agents ^[16] that find usage in many fields (Figure 2).

Figure 2. The industrial application of polymers with antibacterial activity.

The factors that are of the greatest influence on the antimicrobial properties of bioactive polymers are their low toxicity towards human cells and high activity in fighting bacteria cells ^[17]. The mechanism of antibacterial activity of these compounds is provided by active and passive ways of interacting with pathogens ^[18]. The active mechanism of disrupting the function of bacteria cells consists of the destabilisation of bacteria cells through electrostatic interactions between the predominantly hydrophobic and negatively charged bacteria plasma membrane, and the positively charged surface of the modified cationic polymer ^[19]. The most popular active substances used to modify the surface of polymers are quaternary ammonium salts, which interact with the negatively charged membranes of bacteria, causing leakage of components out of the bacterial cell, and consequently, the cell’s death ^[20]. Similar mechanisms of active functional disturbance by electrostatic interaction are exhibited by polyethylenimines. Another example of modifiers on the polymer surface are polyguanidines, which inhibits the bacterial growth due to it breaking the Ca²⁺ salt bridges and N-halamine, which disrupts the function of the amino cell receptors in bacteria by generating the oxidative halogen ^[21]. The passive mechanism of fighting bacteria cells relys on the synthesis of the passive polymer layer, which prevents the adhesion of bacteria on the modified polymer surface, thereby repelling the bacteria without any active interaction with them ^[22].

The natural polymers have a great advantage over the synthetic ones due to their non-toxicity, biocompatibility, non-immunogenicity, and high stability. On the other hand, they are less effective in biomedical applications in comparison to synthetic polymers ^[23]. The modifications that provide the natural polymers with desirable industrial activity include chemical treatment processes such as hydroxylation, carboxylation and epoxidation, or in vitro enzyme treatment ^[24].

Synthetic polymers frequently used in the synthesis of polymers with antimicrobial activity are based on poly(lactic acid) (PLA), polyethylene glycol (PEG), and polyamides ^[25].

2.1. The Medical Application of Polymeric Materials with Antibacterial Activity

The polymers with antibacterial activity are applied in medicine as drug carriers. The encapsulation of the drugs into micelles, nanogels, or vesicles ^[26] not only allows it to curb the bacterial resistance to antibiotics, but also increases the bioavailability of the drug compared to the same conventional antibiotic.

For medical purposes, natural (alginate), artificial (CTS, ethyl cellulose (ET)), and synthetic (PCL—poly(epsilon-caprolactone), PDLA—poly(D-lactide), PGA—poly(glycolide), PLA, PLGA—poly(lactic-co-glycolic acid) polymers are used. The choice of polymer applied as a drug carrier is determined by required residence time and administration site in human cells ^[27]. In addition, the toxicity and tolerance of the polymer carriers in the relevant cell type is assessed.

The polymers applied in drug delivery systems should have hydrolytically or enzymatically cleavable chemical bonds that provide biodegradability in the body, although the non-biodegradable polymers such as polymethacrylates also constitute a promising alternative ^[28]^[29]^[30].

One of the most innovative drug delivery approaches involve the polymer nanoparticles (NPs) ^[31]. The NPs, due to their nanometric dimensions (1–100 nm), are easily accessible to cells and tissues, and deliver a drug straight to the site of action in the human body ^[32]. The NPs are synthetised in the form of nanospheres or nanocapsules. The main difference between them relies on the placement of the carried drug and the mechanism of drug incorporation. The nanospheres are colloidal particles, which adsorb the drug molecule on the particle surface, while the nanocapsules take the form of surrounded polymer shell vesicles with the core filled with aqueous or oily liquid in which the drug is dissolved ^[33]. Among the nanocapsules, dendrimers, micelles, liposomes, and polymersomes are used as nanoparticles to deliver drugs, including antimicrobials ^[34]. Lipid constructs called liposomes are composed of bilayers made of amphipathic lipids. Natural liposomes can be found and isolated from the cells, but synthetic liposomes also are commercially available. Due to the presence of the aqueous phase inside and between the lipid bilayers, they can deliver both lipophilic and hydrophilic drugs to human cells ^[35].

Dendrimers, synthetised for the first time in 1978 by Vögtle et al., are the smallest among the NPs, with a diameter between 1–10 nm. They are obtained in the reaction of protection–deprotection synthesis of the hyperbranched macromolecules, followed by the elongation of the bioactive site from the multifunctional core molecules ^[36]. Dendrimers are particularly interesting as drug carriers due to their amphiphilic structure, globular shape, low dispersity, and highly branched three-dimensional structure ^[37]. The bioactive sites of dendrimers are formed by their surface functional groups, and can be modified with biologically active antimicrobial groups, which provide antimicrobial activity to the polymer ^[38]. The interaction between the bacterial cell and the modified dendrimer surface take place through the electrostatic interactions. Negatively charged bacterial cells interact with positively charged dendrimer functional groups, increasing the permeability of the cell membrane and contributing to the biocidal effect ^[39]. PAMAM—poly(amido)amine, dendritic polylysine, and polypropylenimine (PPI) ^[40] are the most popular, commercially available dendrimers with a cationic surface.

Polymersomes are amphiphilic bilayer vesicles made of tri- or di-copolymer blocks, whose properties are crucial for the overall features of the obtained vesicle. In comparison to liposomes, the polymersomes exhibit greater structural and mechanical stability ^[41]. However, the mechanism of drug transportation is similar—the water-soluble molecules are carried in the inner space of vesicle while the hydrophobic molecules are transferred in the bilayer ^[42].

Polymer micelles are vesicles with a lipophilic core in which only the hydrophobic drugs can be encapsulated, and a hydrophilic shell ensures water solubility of the entire particle. On the contrary to polymersomes, micelles are not able to transport the hydrophilic drugs ^[43]. Figure 3 shows a schematic representation of various drug nanocarriers.

Figure 3. The schemes of polymer nanoparticles. Blue colour represents the hydrophilic part of the NPs; red colour represents the hydrophobic one. The space in which the drugs are introduced is marked in yellow.

Polymer nanoparticles in combination with antibiotics can also be used as synergistic or additive agents to chemically or physically weaken the bacteria via the use of elevated temperatures or the formation of reactive oxygen species. Gold NPs, thanks to their high photothermal efficiency in the presence of near-infrared radiation, are of particular clinical interest because exposure of bacteria to temperatures in the range of 45–50 °C causes a strong antibacterial effect in the body in the form of an increase in the level of cytokines and the body’s cellular immune response. The photothermal NPs may be incorporated in the structures of microneedle (MN) arrays, enhancing the antibiotic delivery directly to the site of infection. MNs are obtained from soluble polymers, making them suitable for delivering antibiotics in a humid environment, and providing high local concentrations of antibiotics to infected cells of the human body. Among the antibiotics successfully delivered by the MNs are vancomycin, polymyxin, tetracycline, chloramphenicol, clindamycin, cephalexin, doxycycline, and gentamicin. Further examples of NPs exhibiting a synergistic effect with antibiotics are tetracycline, chloramphenicol, and rifampicin, which are N-alkylaminated CTS NPs that showed high efficiency against Gram-negative bacteria (E. coli, S. typhimurium). In comparison to metal NPs, these natural mucopolysaccharide NPs are considered more biocompatible and biodegradable, but at a concentration higher than 200 mg/L, chitin nanoparticles exhibit cytotoxic properties ^[44]. Photothermal antibacterial treatment gained recognition due to the reduction of side effects in tissues, low toxicity, high selectivity, and the lack of drug resistance ^[45]. One of the main disadvantages of photothermal treatment of bacterial infections is the necessity for application at a high temperature to make this treatment efficient against drug-resistant bacteria. In order to eliminate this issue, the photothermal treatment can be replaced with chemodynamic therapy with a synergistic effect. The environment of the infection site is characterized by a low pH and overexpression of H₂O₂, which allows for precise targeting of the drug. The application of the silver-doped polyoxometalate (AgPOM) injectable in situ hydrogels are one of the most direct infection-targeting methods, featuring good tissue adhesion, a long-lasting effect, good repeatability, and great photothermal performance ^[46]. Wounds infected with bacteria can also be successfully treated by using hydrogels prepared from poly(aspartic acid) modified with a quaternary ammonium compound/boronic acid cross-linked with poly(vinyl alcohol) polymers. These hydrogels reduced epidermal bacterial survival to 2.3% with an optimal healing rate of 92% after 7 days ^[47].

2.2. Polymer Materials as Antifouling Agents

Apart from drug delivery and antibacterial treatments, the natural and synthetic nanocomposites are applied in cancer therapy, dental applications, and tissues engineering ^[48].

Bacterial infections, apart from mechanical damage, are one of the main causes of transplant failures. Polymeric biomaterials are often used as an antibacterial surface in regenerative medicine, and as the coating for medical implants that prevent bacterial biofilm generation. Bacterial biofilm formation is a defence mechanism against host immune cells, ensures chronicity of infection, and is initiated by a bacterial recognition known as quorum sensing. According to statistics, as much as 80% of clinical infections in humans are caused by biofilms. The presence of biofilm is often observed on the surface of orthopedic screws made of stainless steel and titanium. A mechanism of biofilm formation is presented in Figure 4. The first step is the bacteria;s adhesion to the surface. At a distance of about 50 nm from the implant surface, bacterial cells are attracted by Van der Waals forces. At a distance of 20 nm, between the bacteria and the implant, electrostatic repulsive forces occur depending on the interaction between the surface and the usually negatively charged bacteria. At 5 nm from the surface, the strongest Van der Waals and electrostatic forces, as well as hydrophobic and site-specific interactions, begin to occur. After adhesion to the surface, bacteria start to proliferate and grow, producing extracellular polymeric substances that help them capture nutrients and improve their survivability. Due to the cell–to–cell communication in biofilm, bacteria are able to adapt to environmental conditions and colonize new surfaces. After biofilm maturation, some of it dissipates, releasing floating bacteria that can redeposit on the surface ^[49]^[50]^[51].

Figure 4. The scheme of biofilm formation. Arrow describes the circulation of bacteria cells.

Among the polymeric materials that can be helpful in preventing biofilm formation are antifouling polymers, which repel the bacteria from the surface with chemical or physical mechanisms, and antibacterial ones, e.g., peptide mimetic polymers and cationic polymers ^[52]. Within the antifouling agents, the surfaces functionalised with hydrophilic, zwitterionic, and superhydrophobic polymers should be listed ^[53]. The feature of hydrophilic polymers is their favourable interaction with water, which provides them good solubility and swellability ^[54]. In transplantology, hydrophilic polymers are of great interest due to their ability to mimic the properties of natural cartilage ^[55]. Poly (ethylene glycol) (PEG) and poly (acrylamide) (PAM) (Figure 5) are popular representatives of such hydrophilic polymers ^[56].

Figure 5. The condensed formulas of PEG (a) and PAM (b).

An alternative to hydrophilic polymers such as PEG is zwitterionic polymers, which shows better antifouling properties ^[57]. Zwitterionic polymers also exhibit significant chemical and thermal stability, and excellent biocompatibility even in complex surroundings, e.g., serum or blood ^[58]. The structure of these polymers mimics natural compounds occurring in human cells, such as glycine betaine ^[59]. The repeating constitutional units of zwitterionic polymers contain both negative and positive charges which make them electrically neutral and hydrophilic; furthermore, the entire network of such a polymer exhibits the same characteristics (electrical neutrality and hydrophilicity) ^[60]. On the other hand, the hydrophilicity of zwitterionic polymers is one of their greatest disadvantages, as it leads to a strong absorption of water. High solubility in water and susceptibility to hydrolysis limit their ability to form a film, and as a result, it curbs the use of these polymers as antifouling agents ^[61]. To overcome this difficulty, cross-linking molecules such as polydimethylsiloxane (PDMS) are used to form thin zwitterionic films ^[62].

The most popular zwitterionic polymers are polybetaines. The positive charge in their monomeric units is provided by a quaternary ammonium group, while the negative one is related to the presence of the anionic groups such as sulfonates, carboxylates, phosphonates, phosphates, and phosphinates. According to the charge distribution mode, apart from polybetaines, among the zwitterionic materials, the polyampholytes are also distinguished. The main difference between polybetaines and polyampholytes is the position of the charge. Polybetaines have both cationic and anionic groups located on the same monomer unit separated by an alkyl chain, while polyampholytes have their negative and positive charges situated on different monomer units ^[63].

Another type of bacteria-repelling molecule is superhydrophobic polymers, inspired by lotus leaves, covered by hydrophobic wax. The fluorinated silica-colloid-based surfaces are an example of superhydrophobic polymers exhibiting antiadhesive activity towards S. aureus and P. aeruginosa ^[64]. There is also growing interest around titanium-based materials. Their superhydrophobic properties, bioavailability, and favourable mechanical properties make them useful for cardiac implants ^[65]. In orthopaedics and dentistry, the magnesium alloy coated by hydroxyapatite (HA) and stearic acid confer great antibacterial adhesion capacity ^[66]. The polymers applied in regenerative medicine and tissue engineering must cope with the changes of the extracellular environment that accompany physiological and pathological processes.

Chemically synthesized materials that mimic the extracellular matrix (ECM) appear to be a promising approach to imitate the biological activity of cells ^[67]. The ECM are mostly composed of proteins that perform essential functions in biological processes such as enzymatic reactions, immunological response, cells motility, or signal transduction ^[68]. Thus, protein-mimetic polymers offer hope for accessing complex natural mechanisms. The amphiphilic polymers imitating antimicrobial peptides (AMPs) are highly efficient in preventing biofilm formation. One example of AMPs is photoresponsive AMP based on the N-substituted glycine skeleton, which—due to its efficiency, controllability, and high selectivity—has been used in hydrogels and antifouling surfaces ^[69].

Another kind of polymeric material used as an antifouling agent are the cationic polymers mentioned above, which have been proved to exhibit excellent antibacterial properties. In implantology, polyurethane catheters are often used as implantable medical instruments. Unfortunately, their surface is susceptible to the adhesion of bacteria, which necessitates their frequent replacement in order to prevent bacterial infection. To thwart the formation of a biofilm on polyurethane catheters, the surface modification with cationic polymers can be applied. For this purpose, quaternary ammonium compounds or metal ions are used ^[70].

Some examples of a quaternized compound are benzophenone-based esters and benzophenone quaternary amides, which can be cross-linked on surfaces upon UV radiation. These coatings are efficient against the methicillin-resistant Staphylococcus aureus (MRSA), fluconazole-resistant Candida albicans spp., and influenza virus with 100% efficiency ^[71]. A modified (quaternized or alkylated) polyethyleneimine (PEI) is a cationic polymer containing amino- and imino-groups, also known for its antibacterial properties. PEI is positively charged in neutral and basic solutions, having a high zero potential point at pH values up to 10 ^[72].

The cationic polymers can also be obtained in the innovative reaction of photopolymerization. This method is applied to prepare Sulphur-containing polymers, whose monomers are ionized giving a positive charge, which provides the polymer with antifouling properties ^[73].

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Monika Parcheta

Magdalena Sobiesiak

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