Combating Staphylococcus aureus biofilm with Antibiofilm agents as an efficient strategy to control bacterial infection

 

 Aliaa Abdelghafar, Nehal Yousef, Momen Askoura*

Department of Microbiology and Immunology, Faculty of Pharmacy, Zagazig, University, Egypt.

 

ABSTRACT:

Staphylococcus aureus is an important human pathogen that causes a wide range of infectious conditions both in nosocomial and community settings. Biofilms serve to protect S. aureus from host defenses and antimicrobial agents and therefore play a role in Staphylococcus host pathogenesis. Indeed, biofilm-dwelling bacteria are generally able to tolerate much higher concentrations of antimicrobials than their planktonic counterparts. As a result, biofilm-associated infections are notoriously difficult to eradicate. There is an urgent need for alternative approaches to treat biofilm-related infections. In this review, we present various strategies to combat biofilm-related infections such as small molecules, enzyme therapy and vaccines that weaken structure of bacterial biofilm. However, these promising approaches remain to be validated clinically. Therefore, it is anticipated that these approaches will be eventually developed for treatment of problematic biofilm-related infections notably those are caused by S. aureus.

 

 

 

INTRODUCTION:

Staphylococcus aureus is a Gram-positive, non-motile, non-spore forming and facultative anaerobic bacterium¹. S. aureus is a dangerous human pathogen in both community-acquired and nosocomial infections causing both human and animal infections, ranging from mild superficial infections to toxin-associated diseases and severe life-threatening invasive infections². This pathogen can cause a wide variety of infections, which can be divided into three types: (i) superficial lesions such as wound infection, (ii) toxinoses such as food poisoning, scalded skin syndrome and toxic shock syndrome, and (iii) systemic and life-threatening conditions such as endocarditis, osteomyelitis, pneumonia, brain abscesses, meningitis, and bacteremia³. The broad range of infections caused by S. aureus is related to a number of virulence factors that allow it to adhere to surface, invade or avoid the immune system, and cause harmful toxic effects to host⁴.

 

Staphylococcal virulence factors:

S. aureus expresses many potential virulence factors such as surface proteins that promote colonization of host tissues, proteins that promote bacterial spread in tissues (e.g. leukocidin, kinases and hyaluronidase), surface factors that inhibit phagocytic engulfment (e.g. capsule and protein A), carotenoids and catalase that enhance their survival in phagocytes, membrane-damaging toxins that lyse eukaryotic cell membranes (hemolysins, leukotoxin and leukocidin) and exotoxins that damage host tissues or otherwise provoke disease symptoms⁵.

 

The ability of S. aureus to attach to surfaces and develop a matrix-encased community of cells is generally defined as “biofilm”⁶. Biofilm formation is believed to have an important role in the pathogenesis of staphylococcal infections⁷. The importance of biofilm is well recognized in medical and veterinary contexts. Bacteria in biofilm display elevated resistance to antibiotics and disinfectants⁸. Biofilm also contributes to the evasion of immunological defenses as well as to the difficulty of pathogen eradication, often resulting in persistent infections⁹. Numerous studies have investigated surface adhesins, matrix components and transcriptional regulators, all with the goal of better understanding how S. aureus forms a biofilm and with the eventual goal of improving treatment options. The challenge presented by biofilm infections is that these structures are characterized by higher resistance to chemotherapies and host defenses that promote bacterial persistence in host¹⁰.

 

Stages of staphylococcal biofilm formation:

Staphylococcal biofilm formation is thought to occur in four stages: (1) attachment; (2) microcolony formation; (3) maturation; and (4) detachment. During the first stage, free-floating cells attach to an abiotic or biotic substratum such as a foreign body or host tissue. Following this phase, bacteria multiply to form microcolonies, which are defined as small aggregates of cells that contain some matrix material. It is often considered an intermediate stage of biofilm formation that links the attachment step with the mature biofilm^11,12. The continued growth of microcolonies and production of biofilm matrix components result in a significant accumulation of biomass and development of a mature biofilm. This stage has the characteristic surface structure often associated with bacterial biofilms, such as tower formation and water channels, and cells display the maximal level of resistance to antimicrobials. Finally, mechanical and active mechanisms can initiate cellular detachment from the biofilm. During this stage, the biofilm matrix is typically targeted for degradation resulting in bacterial dissemination which allows free-floating cells to reinitiate biofilm development process at new sites. Detachment of biofilm restores bacterial susceptibility to chemotherapies and is an active area of research interest¹³. In biofilm environment, microbial cells are embedded in a matrix composed of a self-synthesized layer of extracellular polymeric substance (EPS). EPS is essentially formed by polysaccharides, proteins, lipids and extracellular DNA (e-DNA) as well as molecules originating from the host, such as mucus and DNA¹⁴.

 

Therapeutic strategies to prevent biofilm formation by staphylococcus aureus:

The increasing incidence of biofilm associated S. aureus infections necessitates the development of novel methods to treat them¹⁵. The main problem associated with staphylococcal biofilms is increased bacterial resistance within biofilms to both antimicrobial agents and host defense mechanisms. This resistance is predominantly effectuated through diffusion barrier action of the polysaccharide matrix¹⁶. Furthermore, bacterial resistance to antimicrobial agents is mediated through a dormant phenotype caused by adaptation to an anoxic environment and nutrient deprivation. As a result, the metabolic levels of bacterial cells are decreased and cell division occurs at radically lower rates, also Producing slow growing cells known as per sister cells that are highly tolerant to antimicrobialagents¹⁷.

 

Three principal strategies have been developed to prevent biofilm formation or target different biofilm developmental stages. The first principal strategy is inhibiting the adhesion of bacteria to living or non-living surfaces at the initial stage, thus reducing the chances of further development and establishment of biofilm. The second strategy is aimed at the disruption of biofilm architecture during the maturation process¹⁸. The third strategy is an anti-pathogenic or signal interference approach which involves the inhibition of quorum-sensing (QS). S. aureus coordinates biofilm formation and expression of virulence factors via QS to enhance their ability to survive in a specific environment¹⁹.

 

1.     Inhibition of bacterial attachment:

S. aureus biofilm development is associated with major four broad phases, namely; attachment or adherence, microcolony formation, maturation and dispersal. However, the mechanism of the first phase may depend on whether S. aureus attaches to an abiotic or biotic surface²⁰. Bacterial attachment to surfaces is mediated by many factors such as adhesion surface proteins, pili or fimbriae, and specific exopolysaccharides²¹. In general, adhesion occurs most readily on surfaces that are rougher, more hydrophobic, and coated with surface conditioning films²². S. aureus adherence to biotic surfaces depends on the microbial surface component recognizing adhesive matrix molecules (MSCRAMMs) (the largest class of surface proteins anchored to cell wall peptidoglycan) recognition of host proteins²⁰. Thus, abiotic attachment is facilitated by Van der Waal’s forces, electrostatic and steric interactions²³. Altering surface properties of indwelling medical devices such as coating with bactericidal or bacteriostatic substances could prevent biofilm-associated infections²⁴.

 

1.1. Nanotechnology:

It has been shown previously that nanotechnology is a promising approach to treat biofilm-associated infections. Nanoparticles (NPs) are emerging as potential drug delivery systems due to their ability to maintain a sustained drug release at target sites, minimizing side effects and improving the therapeutic efficacy²⁵. Additionally, some nanoparticles are being extensively studied for their intrinsic antimicrobial activity. For instance, metallic NPs can be applied as drug delivery systems as they can protect drugs till being delivered to their target site and avoid immune system activation with low cytotoxicity²⁶. The antibacterial and antibiofilm properties of nanostructured materials are highly influenced by particle size²⁷, shape²⁸, surface charge²⁹ or composition, and the mechanism of nanoparticle as antibiofilm is believed to involve cell membrane alterations³⁰, loss of respiratory activity³¹, lipid peroxidation³², generation of reactive oxygen species (ROS)³³, interference with DNA function and structure³⁴, nitrosation of protein thiols³⁵ or disruptions of metabolic pathways³⁶.

 

It has been established that metal-based NPs have much better antimicrobial activities than their micro-sized counterparts³⁷. For instances Copper, gold, silver, titanium, and zinc have both antibacterial and antibiofilm properties, which could offer alternatives to antibiotics without increasing the risk of resistance development³⁸. In addition, the antibacterial activities of metal oxide NPs have also been studied; examples include zinc oxide (ZnO), copper oxide (CuO), titanium dioxide (TiO₂), iron oxide (Fe₂O₃), cerium oxide (CeO), magnesium oxide (MgO) and aluminum oxide (Al₂O₃)³⁷.

 

One of the most important used Nanoparticle as antibiofilm agent is ZnO. ZnO NPs were synthetized by co-precipitation and evaluated for their antibacterial and antibiofilm activity against S. aureus and P. aeruginosa. ZnO NPs have been found to possess a higher efficiency against established biofilms by both species. The antibiofilm and antibacterial Activity of ZNO NPs is thought to be due to production of ROS that negatively affect bacteria³⁹. In addition, ZnO NPs have been found to have better antibacterial activities and low toxicities in mammalian cells in addition of being highly effective at inhibiting biofilm formation by many pathogens such as E. faecalis, S. aureus, S. epidermidis, B. subtilis and E. coli when compared with NPs of other metal oxides^37,40.

 

1.2. Small molecules:

Small molecules such as aryl rhodanines specifically inhibit biofilm formation by Gram-positive pathogens including S. aureus, S. epidermidis and E. faecalis. Aryl rhodanines are considered potent inhibitors of biofilm formation by staphylococci and enterococci as they inhibit initial adherence of bacterial cells to surface; the initial step of biofilm formation. interestingly, these molecules do not affect planktonic bacterial cells and are not cytotoxic. These molecules lack antibacterial activity and therefore there is no chance to develop bacterial resistance against them⁴¹. Another example for small molecule is calcium chelators such as ethylene glycol tetraacetic acid (EGTA) and trisodium citrate (TSC). The use of chelating agents such as TSC has been shown to disrupt bacterial adherence on synthetic surface, and can help prevent catheter colonization⁴².

 

Abraham et al. showed that there are variable responses by S. aureus towards EGTA and TSC⁴³. In some strains, the chelators prevented bio film formation, while in others, they had no effect or actually enhanced biofilm formation. The mechanism of action of calcium chelators is thought to decrease calcium concentration, and biofilm formation depends largely on clumping factor B (ClfB) which enhances biofilm formation in presence of calcium, consequently biofilm formation would be inhibited⁴³.

 

2.     Disruption of biofilm architecture:

Bacteria within mature biofilms are tolerant to antimicrobial agents due toaltered bacterial growth rate and emergence of resistant subpopulations⁴⁴. In addition, biofilms also promote horizontal transfer of antibiotic resistance genes⁴⁵.

 

2.1. Small molecules:

Many small molecules have been shown to have the potential to disrupt biofilm. For example, Cis-2-decenoic acid (C2DA) is a medium-chain fatty acid chemical messenger produced by P. aeruginosa that can induce dispersion in biofilms in S. aureus, in addition to other Gram-positive and Gram-negative bacteria⁴⁶. In addition to dispersing already formed biofilms, C2DA has the ability to prevent biofilm formation. This potential bio film-preventative characteristic could make it useful asan adjunctive therapy for infection prevention. Furthermore, since antibiotics have been less effective against bio film associated bacteria, C2DA could improve the efficacy of antibiotics in preventing or treating biofilm-associated infections. It has been reported that C2DA could inhibit biofilm in methicillin-resistant S. aureus (MRSA) but is unable to eliminate it completely⁴⁶.

 

2.2. Matrix-target enzymes:

Disruption and degradation of staphylococcal biofilm components such as polysaccharide, eDNA and proteincan weaken and disperse biofilm⁴⁷. Dispersin B which is an enzyme produced during biofilm formation of Gram-negative periodontal pathogen Actinobacillus Actinomycetecomitans could disperse biofilm of some staphylococcal strains⁴⁸. Dispersin B depolymerizes poly-N-acetylglucosamine (PNAG) that plays a vital role in biofilm formation and accumulation and protects the pathogen from the innate host defense⁴⁹. Dispersin B was found to be capable of increasing both antibiofilm and antimicrobial potential of cefamandole nafate (CEF) antibiotic. Dispersin B promotes diffusion of CEF into bacterial clusters and enhances antibiotic delivery to bacterial cell⁵⁰.

 

Other examples of matrix-targeting enzymesare lysostaphin and DNaseI. Lysostaphin is a glycylglycine endopeptidase which could disrupt extracellular matrix of S. aureus biofilms by hydrolysis of pentaglycine cross-bridge in the staphylococcal peptidoglycan. Lysostaphin significantly reduced biomass thickness when applied in vitro to S. aureus biofilms⁵¹. Moreover, Kokai-Kun et al. reported that lysostaphin is an effective treatment for already established biofilm infections on implanted jugular veins catheters in mice, particularly when used in combination with nafcillin⁵².

DNaseI breaks down eDNA in the biofilm matrix and prevents biofilm formation on abiotic surfaces, such as plastic, glass, and titanium surfaces⁵³.

 

2.3. Bacteriophage therapy:

Treatment of biofilm associated-infections using phages offers many advantages, that is, they are highly specific, inexpensive, do not affect normal microflora of the environment to which they are introduced in addition they could improve treatment of infections with conventional antibiotics⁵⁴. Phage may carry specific enzymes on their surface that efficiently degrade bacterial polysaccharides and damage biofilm integrity⁵⁵. SAL-2 (cell wall-degrading enzyme) obtained from S. aureus bacteriophage SAP-2 exhibits a specific lytic activity and can effectively remove S. aureus biofilms⁵⁶. Another example, SAP-26 which was obtained from a clinical strain of S. aureus showed a wide spectrum of lytic activity against both methicillin-susceptible S. aureus (MSSA) and (MRSA)⁵⁷.

 

3.     Signal transduction interference:

Quorum sensing (QS) depends on a series of events including signal production, detection and gene activation/inactivation. Disruption of any of these steps could render the QS to fail and potentially cause defect on the survival and pathogenesis of bacteria^58,59. S. aureus controls biofilm formation and dispersal through the agr QS system. Inhibition of agr makes S. aureus more adherent due to increased biofilm formation. While glucose depletion or addition of autoinducing peptides (AIP) reactivates agr in established biofilm, leading to disassembly and conversion of biofilm-associated cells back to a planktonic phenotype⁶⁰. Activation of the agr system results in increased levels of staphylococcal proteases that cut cell surface proteins and disrupt cell-cell interactions within biofilm leading to bio film dispersal. Moreover, agr activation could induce expression of phenol-soluble modulins (PSMs), which have recently emerged as a novel toxin family that play a role in biofilm development and dissemination of bio film associated infections⁶¹.

 

3.1. Quorum-sensing inhibitors (qsi):

The mechanisms of action of QSI were generally suppression of signal generation, disruption of QS signals and blockage of signal receptors. Bacteria do not die directly from the effects of QSI; thus, there could be less selection pressure and less likelihood of resistance development⁵⁸.

 

The reported QSI whether natural or synthetic can be classified into non-peptide small molecules, peptides and proteins. For example, hammelitannin (HAM), a non-peptide analogue of the quorum-sensing inhibitor RNAIII inhibiting peptide (RIP), was found to reduce S. aureus attachment in vitro and in vivo^62,63. Combination between HAM and clindamycin or vancomycin shows a synergistic effect, by increasing the efficacy of the antibiotics against biofilm-related infections⁶⁴. Similarly, combination between RIP with conventional antibiotics enhances activity of vancomycin, imipenem and ciprofloxacin in treatment of catheter-related S. aureus infections⁶⁵. Finally, an antibody against S. aureus quorum-sensing peptide AP4 was reported to suppress S. aureus pathogenicity in mouse abscess infection model⁶⁶.

 

3.2. Plant-derived natural compounds:

Because of incomparable structural diversity, natural compounds have played an important role in discovering of new drugs⁶⁷. Developing of new drugs from plants could help treatment of persistent infections and inhibit bacterial biofilm formation. For instance, extracts from Krameria, Aesculus hippocastanum, and Chelidonium majus yielded four compounds, namely chelerythrine, sanguinarine, dihydroxy benzofuran and proanthocyanidin, which efficiently inhibit biofilm formation by S. aureus⁶⁸. Proanthocyanins (PAC) active constituent of American cranberry (Vaccinium macrocarpon) was shown to inhibit growth and biofilm formation of Gram-positive bacteria, including Staphylococcus spp. but not the Gram-negative bacteria such as E. coli⁶⁹. Payne et al. reported that tannic acid (polyphenolic) also inhibits S. aureus biofilm formation in various biofilm models without inhibiting bacterial growth⁷⁰.

 

Tea-tree oil, an essential oil extracted from Melaleuca alternifolia eradicates bio film in S. aureus, including MRSA through destruction of ECM and sub sequent removal of the biofilm from surface⁷¹. Tea-tree oil was shown to cause disassembly to pre-established biofilm through damage of adherence factors that are responsible for attachment of bacteria to solid substratum⁷².

 

SUMMARY:

Biofilm infections are considered a great challenge in the medical field. Bacteria within biofilms are highly resistant to both antimicrobial treatment and host immune defense. Therefore, it is essential to introduce other effective ways to overcome these problematic infections. Antibiofilm agents could play a significant role in combating infections caused by biofilm forming bacteria including staphylococcus infections. Herein, different classes of antibiofilm agents and their mechanism of action have been discussed. It is essential to discover new antibiofilm molecules in addition to modification of already known drugs in order to enhance their activity. Finally, in vivo characterization of these antibiofilm agents is essential and would accelerate advances achieved in the battle against bacterial infections.

 

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Received on 06.04.2020           Modified on 21.05.2020

Accepted on 10.07.2020         © RJPT All right reserved