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Biofilm structures are communities that emerge from microorganisms adhering to a surface and living in an extracellular polymer matrix (biofilm matrix). Biofilm formation is affected by various factors, such as strain type, the presence of other bacteria, extracellular polymeric substances, cell adhesion molecules, environmental conditions (such as temperature, pH, salt, relative humidity, oxygen availability, and nutrients), surface properties (such as carrier interface, hydrophobicity, wettability, and roughness), bacterial genome, hydrodynamic conditions, physicochemical properties, cell-to-cell signaling (quorum sensing), bacterial motility. Biofilm can form on the surfaces of devices used in the food and medical sectors (such as stainless steel, glass, and polyurethane) and cause device-related infections. This study presents the factors affecting biofilm formation and on which surfaces the biofilm structure is formed, especially in the food and medical sectors. Identifying the internal and external factors that influence the biofilm life cycle allows for the identification of current strategies for promoting the formation of beneficial biofilms and eliminating harmful biofilms.
Department of Medical Services and Techniques, Program of Medical Laboratory Techniques, Gazi University, Vocational School of Health Services, Ankara, Turkey
*Address all correspondence to: tugbakilic@gazi.edu.tr
1. Introduction
Biofilms are bacterial communities embedded in a matrix formed by the adherence of planktonic cells to a surface and the synthesis of extracellular polymeric substances (EPS) by these attached cells [1]. The biofilm structure forms the living space of 95% of bacteria [2]. EPS in the biofilm layer constitutes the biofilm matrix [3]. The EPS matrix involves primarily extracellular polysaccharides (exPs) and contains smaller amounts of other biopolymers, including extracellular proteins (exPr), extracellular DNA (eDNA), and extracellular lipids (exLp). The macromolecular content of EPS varies depending on the diversity of microorganism species and the growth conditions of the cell [1, 3, 4]. These different EPS matrix components come together and interact. The EPS matrix is affected by various intrinsic (strain type, genotype, etc.) and extrinsic factors (surface properties, environmental conditions, fluctuations in nutrients, physicochemicals, etc.) [5, 6]. These internal and external factors combine to produce a dynamic and heterogeneous microenvironment [5]. Moreover, microbial adhesion to surfaces is a complex process involving physicochemical, exPs, and exPr factors [7]. This inherent complexity can make the isolation and characterization of matrix components difficult [5].
Planktonic cells can attach to a surface. In this initial phase, the attachment is easily reversed but becomes strong and irreversible. Cell growth and division form a biofilm layer found everywhere life can exist [8]. Biofilm formation occurs naturally due to the balance between various chemical, physical, and biological processes [9]. Bacteria can be planktonic (free-living), but in most natural ecosystems, they prefer to grow as biofilms (sessile) at interfaces. This may be due to the nutrient concentration of the interface or adaptation to harsh conditions [8]. Biofilms in natural environments often maintain homeostasis under fluctuating and harsh environmental conditions [10]. Furthermore, biofilm formation is a survival mechanism for microorganisms and an adaptation strategy to adverse environmental conditions [6]. In addition, the EPS matrix plays an important role in bacterial physiology and ecology. These properties include structural protection, cellular interaction, nutrient utilization, horizontal gene transfer, and adaptation of bacterial populations to the environment. The matrix content varies depending on the bacterial species and the interface where the biofilm is formed. Cell migration to this interface can occur by passive mechanisms or by internal interactions of planktonic bacteria [1]. Biofilm-forming bacteria have advantages such as a greater abundance of nutrient molecules, protection from antibiotics, disinfectants, and dynamic environments, synergistic growth and survival in nutrient-deficient conditions, modification of their metabolic activities, stabilization of enzymes, promotion of ion exchange and a protective barrier formed by the EPS matrix they generate [11, 12].
Some biofilms contain only a single species, while others contain many species [13]. However, biofilms formed by multiple bacterial species are more common in the natural environment due to their ecological advantage. Mixed-species biofilms are generally more resistant to antibiofilm agents than monospecies biofilms [6]. In mixed-species biofilms, each type of component may produce different polymers. The physicochemical properties of such a biofilm matrix may differ significantly from those of purified components. Additionally, EPS components from two or more species may interact synergistically, increasing bacterial adhesion [5]. Production of EPS, such as surface-associated polysaccharides and proteins, may give a microorganism a competitive advantage in a mixed microbial community [9]. Moreover, dual-species biofilms can gain unique properties compared to their respective monoculture colonies [14]. The function and chemical compound of exPs may vary depending on the bacterial species or strain [1].
Microbial contamination on different surfaces can adversely affect human health and the environment. It can lead to significant problems in various technologies, such as food, medical, and service sectors [15, 16]. Contamination can occur at any stage of food processing industries, such as through contact of contaminated food with surfaces or food equipment. In addition, contaminants can contaminate surfaces and devices such as surgical instruments, ventricular-assisted devices, vascular catheters, urinary tracheal intubation, catheters, respiratory systems, endoscopes, orthopedic implants, pacemakers, mechanical heart valves, and needles. These contaminants can cause both food-related and healthcare-associated infections [17, 18, 19]. Understanding the relationship between surface conditions and microbial adhesion enables the improvement of new strategies to prevent bacteria and spores from adhering [15].
To prevent contamination and offer solutions different from current strategies against infections, revealing the factors that microorganisms need to form biofilms is a substantial step. If the mechanisms of surface attachment between planktonic and biofilm life forms, specific to the microorganism species, can be comprehensively explained, then we will be one step closer to the discovery of effective, cheap, and environmentally friendly biofilm prevention agents. In this context, this study aims to reveal which factors affect a microorganism’s ability to form biofilms and discuss biofilms’ importance in the food and medical sectors.
Biofilms are considered responsible for food spoilage, epidemics, and damage to food processing equipment. Therefore, it is necessary to be well-informed about all the factors that affect the development or growth of bacteria (Figure 1), including the attachment surface, environmental conditions, associated bacterial cells, and electrostatic charging of the surfaces [28]. Bacterial extracellular surface components and environmental signals are vital for autoaggregation and biofilm formation. Due to their strategic location on the cell surface, outer membrane proteins, lipopolysaccharides, and proteinaceous structures such as pili and fimbriae are known to influence bacterial adhesion and autoaggregation phenotype [1, 29].
Microorganisms usually adhere fast to surfaces in which they come into contact [11]. In the biofilm life cycle, initial attachment occurs rapidly via physicochemical interactions between the surface and bacteria. Within a short time, gene expression changes, and biofilm structure growth begins as cells are physically attached to the surface by the EPS [17, 30]. Furthermore, the nonspecific adhesion of microorganisms to surfaces is a physicochemical phenomenon and results from electrostatic and non-electrostatic interactions between the surface of the solid and the bacteria. When electrostatic double layers connected by charged groups on each surface come into contact, electrostatic forces are generated between the microorganism’s surface and the receiving surface. Covalent bonding, Van der Waals forces, acid-base and metallic interactions, and ionic bonding are the forces that play a role in non-electrostatic interactions [11]. To reduce or prevent microbial adhesion, it is important to know the physicochemical surface properties of microorganisms, such as Lewis acid-base or electron acceptor/electron donor character [31]. Liquids and polymer surfaces can contain three types of hydrogen-bonding molecules: (a) proton acceptors (electron donors or bases) (polystyrene and polycarbonate etc.), (b) proton donors (electron acceptors or acids) (polypropylene and polyvinyl chloride etc.), and (c) proton acceptors and donors (polyamides, polyimides, and polyvinyl alcohol etc.) [32]. In addition, bacteria may initially attach to the surface via flagella, pili, and fimbriae [33]. However, in a study, a swimming motility test revealed no relationship between the initial adhesion and motility of Listeria monocytogenes. In contrast, the cellular hydrophobicity of L. monocytogenes was shown to be an important feature in the initial adhesion to polyvinyl chloride and biofilm formation [34].
Depending on the type of interaction, the attachment to the surface may be transient or permanent. Under environmental conditions, bacterial cells may become irreversibly attached to the surface via surface adhesins. While adhesion to abiotic surfaces is generally mediated by nonspecific interactions, adhesion to biotic surfaces typically requires a specific receptor-adhesin interaction [30]. Zeta potential measurements have shown that most bacteria have a negative charge, so they will bind quickly and tightly to positively charged surfaces [35]. A hydrophobic surface, such as plastic, has a lower repulsive force than a hydrophilic surface, such as glass and metal. The decreased repulsive forces correspond to increased adhesion forces [13]. Moreover, microbial cells encounter repulsive hydrodynamic forces near the surface in a liquid environment. Bacteria often use cell surface organelles such as flagella or pili to overcome these repulsive barriers. When bacteria adhere to the surface, binding can be increased via adhesins, and irreversible binding can be triggered [30]. Motility via flagella can occur through free cells “swimming” in aqueous environments or bacterial populations “swarming” on solid, moist surfaces. If the bacteria do not have motility organelles, surface proteins play a role in initial attachment to the surface [1].
Microorganisms can communicate with each other. Cell communication is usually achieved by diverse chemical signaling molecules (autoinducers) produced and released by bacteria. In this process, called Quorum sensing (QS), bacteria communicate with each other via autoinducers to regulate their gene expression in response to fluctuations in bacterial cell population density [10]. QS is vital in regulating biofilm formation and its virulence [13]. QS regulates all the stages of biofilm formation [33]. Furthermore, QS modulates various cellular functions, including pathogenesis, obtaining nutrients, conjugation, motility, and secondary metabolite production [35]. Two types of QS systems are recognized in bacteria: intraspecific and interspecific communication. Intraspecific and interspecific interactions between microorganisms can be either antagonistic (such as competition for nutrients or inhibition of growth) or synergistic. Bioluminescence, virulence factor expression, antimicrobial resistance, sporulation, and maturation of microorganisms depends on complex interactions [36]. QS molecules, called autoinducers, consist of N-acyl homoserine lactones (AHLs), oligopeptides, and autoinducer-2. AHLs and oligopeptides are QS molecules in intraspecies communication in Gram-negative and Gram-positive bacteria, respectively. Autoinducer-2 is an interspecies communication signal in Gram-positive and Gram-negative bacteria [37]. It has been demonstrated that the QS system is required for full virulence of many important pathogenic organisms such as Pseudomonas aeruginosa, Staphylococcus aureus, Burkholderia pseudomallei, Burkholderia cenocepacia, and Vibrio cholerae [38]. The las system is a QS system that controls different physiological functions in response to cell density in many bacteria. P. aeruginosa requires the las QS signaling system to form biofilm. This system controls the synthesis of the intercellular signaling molecule N-(3-oxododecanoyl)-L-homoserine lactone [20]. The Burkholderia cepacia complex (Bcc) comprises opportunistic bacterial pathogens. These species cause cystic fibrosis and immunosuppression. These bacteria can use two chemical languages: AHLs and cis-2-unsaturated fatty acids [39].
Bacteria that form biofilms compete for nutrients and habitat. This competition can result in the production of toxins that aim to inhibit or kill neighboring cells. Additionally, bacteria can adapt to nutrient depletion and other environmental stresses by regulating their metabolism, gene expression, and protein synthesis, often resulting in reduced cell division rates and metabolic activity. Differential growth rates and gene transcription among biofilms result in distinct phenotypes that determine their characteristics [40]. Monospecies biofilm communities often consist of phenotypically distinct subpopulations. The differentiation of biofilm cells may depend on the environmental conditions surrounding the cells. Different concentrations of oxygen, nutrients, ions, and chemicals create various microhabitats that provide favorable conditions for bacterial colonization [10]. Furthermore, biofilm formation is a multifactorial process that involves the properties of the bacterial cell and the biological, chemical, and physical properties of the biomaterials relative to their surface. The microbial adhesion factors are not yet fully understood [41]. However, it is known that environmental factors such as temperature and pH affect biofilm formation and can facilitate bacterial adhesion. Environmental factors regulate biofilm formation in several pathways. Mature biofilms adapt to environmental conditions to obtain the best nutrients for survival and reproduction [33]. Nutrient deficiencies or low nutrient conditions stress microorganisms and trigger biofilm formation. However, if nutrient levels are consistently low, biofilms cannot mature [13].
Biofilm formation is a bacterial stress response to environmental conditions. In one study, the effects of different temperatures, pH, salt, glucose, and lactose concentrations on the biofilm cells of Lactococcus lactis subsp. lactis KGPMF23 and Lactobacillus fermentum KGPMF29 were examined. All tested glucose (0.5, 1.5, 2.5, 3.5%) and lactose (0.5, 1.5, 2.5, 3.5%) concentrations showed stimulatory effects on biofilm formation at 37°C. The biofilm formation ability of KGPMF23 was stimulated at 4 and 6.5% salt, while the biofilm formation ability of KGPMF29 was stimulated at all salt concentrations (4, 6.5, and 8%) [42]. Various factors such as temperature, time, substrate type, origin, and nutrient availability affect L. monocytogenes biofilm formation [43]. In Bacillus subtilis, the alternative sigma factor sigma B is activated by stress factors such as temperature, salt, and starvation [14]. The virulence of Staphylococcus epidermidis, such as its ability to produce gelatinase and slime, depends on the host and environmental factors [44]. S. epidermidis and S. aureus biofilms are governed by significant fluctuations in the pH of the medium under adverse conditions [45].
EPS comprises approximately 75–95% of the biofilm volume, with bacteria comprising 5–25% [45]. EPS secreted by individual cells provides advantages to microorganism communities, such as structural integrity and protection from environmental stress [40]. Moreover, the EPS matrix supports microbial growth and development [29]. EPS can vary across species and growth conditions and stimulates chemical communication, formation, and secretion between cells in the microbial community [35]. In addition, EPS can be a nutrient source and electron donor/acceptor for microorganisms. The network of hollow channels between cells enables the exchange of oxygen, nutrients, and wastes [29]. EPS, and in the negative case, it prevents surface colonization due to the toxic effect of some metal ion species such as Cr [3]. The quantity of EPS varies depending on the age of the biofilms, the type of microorganisms, and the environmental conditions [46]. Changes in environmental conditions may cause the phenotype to change from planktonic to biofilm form. Furthermore, environmental conditions can affect bacterial and surface properties. exPs production serves a role in biofilm protection against environmental stress factors [9]. When a bacterial cell attaches to a surface, a series of physiological changes begin and can lead to the overproduction of exPs. These exPs help cells attach to the colonized surface and facilitate the spatial organization of different species within a biofilm [5]. Biofilm formation depends on the chemical environment. Pseudomonas strains can generate different exPs in soil or the human body. Furthermore, changes in biofilm composition have been observed with changing growth stages, alteration of carbon source, water availability, and toxins [47]. S. aureus and S. epidermidis are the predominant contaminants of vascular catheters, and the critical component for surface attachment is polysaccharide intercellular adhesin (PIA) [20]. Some adhesive factors such as aggregation-associated protein (Aap)/biofilm-associated protein (Bap), eDNA, and PIA can stabilize the biofilm. Although exPs are important and often essential components of the biofilm matrix, recent evidence suggests that surface proteins play a leading role in developing microbial communities [21, 33]. The exPr that comprises the EPS matrix is a mixture of secreted exPr, protein subunits of cell appendages (pili and flagella, etc.), cell surface adhesions, and outer membrane vesicle proteins. They interact with exPs and nucleic acid components to help stabilize the EPS matrix, promote surface colonization, and maintain the integrity and architecture of the biofilm [19]. Biofilm-associated proteins are Bap (S. aureus, and B. cepacia), Mus 20 (Pseudomonas putida), VP1443 (Vibrio parahaemolyticus) [21].
Biofilms are assemblages of surface-associated microbial cells [29]. Moreover, bacteria adhere to almost all natural and synthetic surfaces and are vital to survival (Table 1) [48]. Plastic-associated biofilms may have negative effects due to the accumulation of pathogens on the surface and the transfer of resistance genes such as antibiotics and metals [22]. Plastics, such as polycarbonate, polypropylene, polystyrene, polyamides, polyester, polyvinyl chloride, and polyethylene, are synthetic organic polymers, with 100 million tons produced annually worldwide and increasing daily production [29, 59]. In addition, stainless steels are commonly used in the food and beverage manufacturing and processing industries. Different surface properties can determine bacterial adhesion. A study evaluated the surface roughness of stainless steel by 3D polishing, brushing, grinding, and electropolishing. The results showed that the rate of adhering bacteria increased with increasing surface roughness. Bacteria adhere more to rougher surfaces because of increased interaction between the increased efficient surface area and the increased number of cracks, gaps, and spaces [15]. S. epidermidis adhesion to the surface may be related to the stiffness of the polymer substrate. However, the mechanisms that mediate cell surface interaction and the importance of physical properties in cell adhesion may be difficult to understand [35].
Surface types are used in the food and medical sectors.
Stainless steel can be an ideal surface for bacteria to adhere to; still, it is the material most commonly used to make containers, pipes, valves, and different types of equipment in the food processing industry [60] because stainless steel is significantly more biocleanable than glass. Additionally, biofilm-associated microorganisms growing on a stainless steel surface can be killed by lower disinfectant concentrations than those on polymer surfaces. On stainless steel surfaces, it is important to consider the quality and age of the steel, the surface roughness, and the cleaning conditions used [11]. L. monocytogenes can adhere to food-contact surfaces (polystyrene, glass, stainless steel, etc.) and form biofilms [15]. In one study, the surface roughness of materials, including aluminum, rubber, polypropylene, and polycarbonate, varied greatly (0.7–3.5 log10 Ra) and was reported to have a positive correlation with biofilm formation (rs = 0.573) [43]. S. epidermidis is one of the main causes of medical device-related infections, including prosthetic infections [44]. It has been found that most S. epidermidis strains produce more biofilm on acrylic surfaces than on glass. Therefore, a hydrophobic surface has been found to support biofilm formation on most clinical isolates of S. epidermidis [7].
Microbial hydrophobicity is the attractive energy between apolar or slightly polar cells immersed in an aqueous phase. In biological systems, hydrophobic interactions are generally the strongest noncovalent forces, often mediating surface adhesion [7]. Because most interface systems have multiple parameters, it is difficult to evaluate the results of most adhesion tests based solely on hydrophobicity [17]. While spreading, wetting, and adhesion are effective in the interaction of polymer surfaces with liquids (solid polymer-liquid interface), contact adhesion, hardness and scratching, friction, and wear are effective in the interaction with solids (solid polymer-solid interface). A reversible free energy change per unit area of the new interface occurs [32]. Surface-free energy correlates more with the binding force than the number of bacteria attached per unit of surface area [17].
Changes in hydrodynamic conditions can affect the structure of biofilm matrix cells. The shear rate affects the erosion rates of cells in the biofilm matrix [5]. Two mechanisms can lead to cell detachment from the biofilm: increased external shear forces or decreased internal strength [9]. The role of wettability is essential in the attachment of planktonic cells to the hydrophobic and hydrophilic biofilm carrier surface. Wettability can help overcome the electrostatic repulsion during the initial attachment between cells with different affinities (hydrophobicity-hydrophilicity) and the surface. In addition, the wettability of the biofilm colony is a result of multiple interactions with EPS, such as ionic protein, exPs, humic acid, uronic acid, eDNA, and cations. EPS contains both hydrophilic and hydrophobic components. As the biofilm matures, the role of EPS in determining the surface properties and microbial attachment-detachment interactions becomes more dominant. As a result, EPS changes the surface properties and improves cellular attachment. In addition, wettability can affect the initial biofilm attachment rate and the durability of established biofilms. In addition, roughness can increase the wettability of the surface. Rough surfaces are effective in the initial attachment and detachment of cells. Therefore, selecting the optimum roughness is important for balancing the biofilm formation and detachment rate [46]. The importance of fluid hydrodynamics for resistance to external shear forces in P. putida and P. aeruginosa biofilms has been actively studied. Observations indicated that biofilm maturation and distribution are regulated somewhat by shear forces and microenvironmental hydrodynamics [45]. One study reported that cell surface hydrophobicity increased with temperature [50]. On the other hand, it was determined that S. epidermidis hydrophobicity had little or no effect on surface adhesion [7].
Biofilm is a significant concern in several applications, from biomedical implants and devices to food packaging and industrial equipment [61]. Escherichia coli, P. aeruginosa, S. aureus, Streptococcus pneumoniae, and Salmonella typhimurium can cause food poisoning and nosocomial infections [2]. P. aeruginosa is found in humans, animals, abiotic surfaces, food, and medical devices, and its ability to infect increases when it forms a biofilm [16].
3.1 Food sector
In the food industry, sedimentation due to gravity, the dominant mechanism in storage or fermentation tanks, turbulence of the suspension liquid in large pipeline systems, and Brownian motion are factors that initially affect the attachment of microorganisms to a surface [11]. Biofilms have been found on equipment and tools in milk processing plants, including bends in pipes, gaskets, floors, and milk-handling devices [49].
Adequate nutrients on food and food processing surfaces create ideal conditions for microbial growth and attachment [62]. In the food industry, the binding surface properties (hydrophobicity, electrostatic charging, interface roughness, topography, etc.) affect the overall hygiene of the surface as they affect biofilm formation [28]. Microscope analysis has determined that smooth stainless steel surfaces can be damaged by mechanical cleaning and that bacteria and organic residues can adhere to small cracks and scratches formed on the surfaces [50]. Type 304 stainless steel is the most widely used food-contact material in the food industry because it is easy to clean and resistant to extreme corrosion at different processing temperatures [28].
Biofilms can form on processing environment surfaces and food, causing cross-contamination and post-process contamination. Thus, microbial colonization can be found on food surfaces, packaging material surfaces, milk storage tanks and heat exchange equipment [17]. S. aureus is a pathogenic bacterium that forms biofilms on food processing surfaces [50]. Moreover, Streptococcus thermophilus is a well-known contaminant strain of heat exchanger plates in the dairy industry [63]. Bacillus cereus spores in raw milk could remain in heat exchange equipment and grow out, contaminating the product [17]. Furthermore, the commonly isolated pathogens were L. monocytogenes, Salmonella spp., E. coli, Vibrio spp., Campylobacter jejuni, and Clostridium perfringens in the food sector. During milk processing, thermophilic streptococcal strains can adhere to pasteurizers’ heat exchanger plates and lead to pasteurized product contamination, adversely affecting their taste [64].
3.2 Medial sector
Typical biologically important interfaces include the cell surface-synthetic biomaterial, EPS matrix-biomolecule, EPS matrix-cell, hydrated tissue-air (lung), and mineral-protein (bone) [58]. Biofilm may form on biological implants and drug-delivery devices [62, 65]. Biofilm formation after protein adsorption on biological implants reduces the effectiveness of the devices and may lead to harmful side effects such as thrombosis. Biofilm may form at the interface between bone and the implant surface. Moreover, infection around orthopedic implants and in chronic osteomyelitis is associated with developing bacterial biofilm, a barrier to antibiotics. One solution to this problem could be delivering antibacterial drugs by local carriers. The ideal vehicle should provide high local antibiotic concentrations above the minimal inhibitory concentrations for most common pathogens without causing systemic toxicity [65].
The biofilm cells that develop on carrier surfaces are more resistant than planktonic cells in terms of survival mechanisms [46]. In addition, biofilm-associated bacteria may exhibit different characteristics than planktonic cells, such as different physiology, immune system, and high antibiotic resistance, making biofilms a source of chronic and persistent infection [9]. It was observed that P. aeruginosa, which formed a biofilm on the catheter surface, was still viable after 1000 μg/mL tobramycin exposure for 12 hours. Two mechanisms can explain antibiotic resistance. First, the biofilm matrix absorbs and degrades antibiotics, forming a strong barrier and limiting their penetration. Second, bacteria within the biofilm can slow down their metabolism when exposed to antibiotics, thus reducing their uptake and sensitivity to antibiotics [66].
The most common bacterial microorganisms that cause biofilm infections are S. epidermidis, S. aureus, P. aeruginosa, Haemophilus spp., Acinetobacter spp., and Enterobacteriaceae [67]. Moreover, most microorganisms that cause hospital infections are biofilm producers, and due to this ability, they can adhere to abiotic surfaces and cause initial catheter infections and later bloodstream infections. Hospital-acquired infections are associated with medical insertion devices such as intravenous catheters [16]. Infections caused by microbial biofilms include intravascular catheter, prosthetic joint, and implant (such as knee and hip) infections [67, 68]. Intravenous catheter infections frequently lead to bloodstream infections, which can be a significant cause of death and healthcare costs. Furthermore, multispecies biofilms can cause infections in sterile body parts, such as urinary tract infections in patients with urinary tract catheters or ventilator-associated pneumonia in intubated patients [67].
Biofilm is a substantial problem in the medical sector because it forms on medical implants within human tissue and causes many serious chronic infections. Due to their adapted biofilm phenotypes, S. aureus and S. epidermidis are among the most important bacteria causing device-associated infections [16, 62]. Methicillin-resistant S. aureus’s ability to form biofilms on biotic and abiotic surfaces is the primary cause of its antibiotic resistance and pervasiveness [68]. Generally, staphylococci are the most common cause of infections associated with indwelling medical devices [67]. Moreover, coagulase-negative staphylococci can cause endovascular and catheter-related bloodstream infections. The most important virulence factor of S. epidermidis is its ability to adhere to devices and form biofilms [7]. Moreover, S. epidermidis is a significant infectious agent in patients with peritoneal dialysis catheters [44].
Identifying the regulatory mechanisms required for biofilm formation and characterizing the properties of biofilm matrix components are important for biofilm studies [14]. The exact result of some parameters, such as roughness and hydrophobicity, can vary greatly under different laboratory conditions. The lack of clear results may be due to the different methods and bacterial strains [28]. Despite these handicaps, developing methods to prevent biofilm growth and/or formation by harmful bacteria allows the detailed elucidation of the five-stage biofilm life cycle mechanism [2, 23].
The increased use of materials resistant to bacterial adhesion in the food industry can improve food safety [60]. In addition, strong hydrophobic and low-energy surfaces are preferred for biofilm control in industries due to their stability and lower interaction with living cells. Materials with surface energy between 20 and 30 mN/m are reported to be suitable antibiofilm materials [59]. One of the most promising strategies to prevent or delay biofilm formation in medical and industrial environments is to use antiadhesive coatings that release contact killers or biocidal substances. Since medical and industrial biofilms usually develop in areas with fluid movement, studying the environmental conditions during bacterial-surface interactions during initial adhesion is an important step [69]. Knowing the nature of polymers is important for applications such as organic coatings to prevent corrosion [59]. Moreover, different strategies to prevent biofilm include antibiofilm surface coatings as an environmentally friendly alternative. Nontoxic polydimethylsiloxane coatings can create self-cleaning surfaces [70].
Protein-resistant coatings can be used to inhibit bacterial attachment. These coatings can be designed to release biocidal agents (antibiotics, quaternary ammonium salts, silver, etc.) into the surrounding aqueous environment. However, alternative strategies, such as using polycations, enzymes, biocides, nanomaterials, and photoactive agents, should be developed for antibiotic- and silver-resistant pathogen strains. The most widely known photoactive material is titanium dioxide (TiO2), which has a self-cleaning effect. Different types of surfaces, such as glass and catheters, can be coated with TiO2 [61]. Antibiotic doses effective against planktonic forms in vitro are ineffective against the same bacteria in biofilm forms. Therefore, a 200–1000-fold higher concentration of the same antibiotic may be required. Effective doses for biofilm removal may be toxic to the patient [65]. Particulate drug-delivery systems are considered a promising strategy to solve problems associated with antibiotic treatments in biofilm environments [71].
The EPS matrix contains organic molecules as well as inorganic compounds such as metal ions and minerals [14]. Removing metal ions reduces the surface’s chemical reactivity, rendering it less susceptible to bacterial attachment [60]. A common method of biofilm inhibition involves disrupting cellular function with substrate-associated metals. Nanoparticles such as silver are interesting for thermodynamically mediated biofilm inhibition and are more effective when used with a secondary antimicrobial component [2]. In a study, an innovative approach to direct live cell migration on patterned quasi-liquid surfaces was applied and presented as a promising strategy to prevent biofilm formation and combat biofilm-associated infections. This study induced living bacterial cells to aggregate on adhesive patterns [66].
To develop strategic measures such as increasing the use of antifouling surfaces in biofilm control studies, the factors affecting biofilm structure should be addressed individually, and the interaction mechanisms between them should be revealed on a strain-specific basis. In addition, whether there is a difference between the two life forms containing planktonic and biofilm cells in terms of EPS content or other factors should be evaluated in detail. Determining how similar biofilm matrix polymers are to planktonic cell polymers and which polymers are biofilm-specific will bring us one step closer to new biofilm control strategies. Considering biofilm control strategies’ positive and negative aspects, the most effective method for humans and the environment should be selected according to bacterial species.
References
1.Bogino PC, de las Mercedes Oliva M, Sorroche FG, Giordano W. The role of bacterial biofilms and surface components in plant-bacterial associations. International Journal of Molecular Sciences. 2013;14(8):15838-15859. DOI: 10.3390/ijms140815838
3.Beech IB. Corrosion of technical materials in the presence of biofilms—Current understanding and state-of-the art methods of study. International Biodeterioration and Biodegradation. 2004;53(3):177-183. DOI: 10.1016/S0964-8305(03)00092-1
4.Jakubovics NS, Shields RC, Rajarajan N, Burgess JG. Life after death: The critical role of extracellular DNA in microbial biofilms. Letters in Applied Microbiology. 2013;57(6):467-475. DOI: 10.1111/lam.12134
5.Allison DG. The biofilm matrix. Biofouling. 2003;19(2):139-150. DOI: 10.1080/0892701031000072190
6.Sharan M, Vijay D, Dhaka P, Bedi JS, Gill JPS. Biofilms as a microbial hazard in the food industry: A scoping review. Journal of Applied Microbiology. 2022;133(4):2210-2234. DOI: 10.1111/jam.15766
7.Cerca N, Pier GB, Vilanova M, Oliveira R, Azeredo J. Quantitative analysis of adhesion and biofilm formation on hydrophilic and hydrophobic surfaces of clinical isolates of Staphylococcus epidermidis. Research in Microbiology. 2005;156(4):506-514. DOI: 10.1016/j.resmic.2005.01.007
8.Beveridge TJ, Makin SA, Kadurugamuwa JL, Li Z. Interactions between biofilms and the environment. FEMS Microbiology Reviews. 1997;20(3-4):291-303. DOI: 10.1111/j.1574-6976.1997.tb00315.x
9.Alotaibi GF, Bukhari MA. Factors influencing bacterial biofilm formation and development. American Journal of Biomedical Science and Research. 2021;12(6):617-626. DOI: 10.34297/AJBSR.2021.12.001820
10.Dufour D, Leung V, Lévesque CM. Bacterial biofilm: Structure, function, and antimicrobial resistance. Endodontic Topics. 2010;22(1):2-16. DOI: 10.1111/j.1601-1546.2012.00277.x
11.Boulané-Petermann L. Processes of bioadhesion on stainless steel surfaces and cleanability: A review with special reference to the food industry. Biofouling. 1996;10(4):275-300. DOI: 10.1080/08927019609386287
12.Aravinthan A, Arkatkar A, Juwarkar AA, Doble M. Synergistic growth of Bacillus and Pseudomonas and its degradation potential on pretreated polypropylene. Preparative Biochemistry & Biotechnology. 2016;46(2):109-115. DOI: 10.1080/10826068.2014.985836
13.Samrot AV, Abubakar Mohamed A, Faradjeva E, Si Jie L, Hooi Sze C, Arif A, et al. Mechanisms and impact of biofilms and targeting of biofilms using bioactive compounds—A review. Medicina. 2021;57(8):839. DOI: 10.3390/medicina57080839
14.Arnaouteli S, Bamford NC, Stanley-Wall NR, Kovács ÁT. Bacillus subtilisbiofilm formation and social interactions. Nature Reviews. Microbiology. 2021;19(9):600-614. DOI: 10.1038/s41579-021-00540-9
15.Bohinc K, Dražić G, Abram A, Jevšnik M, Jeršek B, Nipič D, et al. Metal surface characteristics dictate bacterial adhesion capacity. International Journal of Adhesion and Adhesives. 2016;68:39-46. DOI: 10.1016/j.ijadhadh.2016.01.008
16.Cangui-Panchi SP, Ñacato-Toapanta AL, Enríquez-Martínez LJ, Reyes J, Garzon-Chavez D, Machado A. Biofilm-forming microorganisms causing hospital-acquired infections from intravenous catheter: A systematic review. Current Research in Microbial Sciences. 2022;3:100175. DOI: 10.1016/j.crmicr.2022.100175
17.Brooks JD, Flint SH. Biofilms in the food industry: Problems and potential solutions. International Journal of Food Science and Technology. 2008;43(12):2163-2176. DOI: 10.1111/j.1365-2621.2008.01839.x
18.Abdallah M, Benoliel C, Drider D, Dhulster P, Chihib NE. Biofilm formation and persistence on abiotic surfaces in the context of food and medical environments. Archives of Microbiology. 2014;196(7):453-472. DOI: 10.1007/s00203-014-0983-1
19.Rather MA, Gupta K, Mandal M. Microbial biofilm: Formation, architecture, antibiotic resistance, and control strategies. Brazilian Journal of Microbiology. 2021;52:1701-1718. DOI: 10.1007/s42770-021-00624-x
22.Bhagwat G, O’Connor W, Grainge I, Palanisami T. Understanding the fundamental basis for biofilm formation on plastic surfaces: Role of conditioning films. Frontiers in Microbiology. 2021;12:687118. DOI: 10.3389/fmicb.2021.687118
23.Kilic T, Bali EB. Biofilm control strategies in the light of biofilm-forming microorganisms. World Journal of Microbiology and Biotechnology. 2023;39(5):131. DOI: 10.1007/s11274-023-03584-6
24.Felz S, Vermeulen P, van Loosdrecht MC, Lin YM. Chemical characterization methods for the analysis of structural extracellular polymeric substances (EPS). Water Research. 2019;157:201-208. DOI: 10.1016/j.watres.2019.03.068
25.Feng J, Ma L, Nie J, Konkel ME, Lu X. Environmental stress-induced bacterial lysis and extracellular DNA release contribute to Campylobacter jejuni biofilm formation. Applied and Environmental Microbiology. 2018;84(5):e02068-17. DOI: 10.1128/AEM.02068-17
26.Zikalala NE, Zikalala SA, Azizi S, Kamika IA, Nxumalo EN, Zinatizadeh AA, et al. The role of inorganic and carbon nanomaterials in surface modification to attain antibiofouling polymeric membranes for water treatment—A review. Industrial and Engineering Chemistry Research. 2023;62(24):9354-9380. DOI: 10.1021/acs.iecr.3c00400
27.Kalia VC, Patel SK, Lee JK. Bacterial biofilm inhibitors: An overview. Ecotoxicology and Environmental Safety. 2023;264:115389. DOI: 10.1016/j.ecoenv.2023.115389
28.Carrascosa C, Raheem D, Ramos F, Saraiva A, Raposo A. Microbial biofilms in the food industry—A comprehensive review. International Journal of Environmental Research and Public Health. 2021;18(04):2014. DOI: 10.3390/ijerph18042014
29.Moyal J, Dave PH, Wu M, Karimpour S, Brar SK, Zhong H, et al. Impacts of biofilm formation on the physicochemical properties and toxicity of microplastics: A concise review. Reviews of Environmental Contamination and Toxicology. 2023;261(1):8. DOI: 10.1007/s44169-023-00035-z
30.Berne C, Ducret A, Hardy GG, Brun YV. Adhesins involved in attachment to abiotic surfaces by Gram-negative bacteria. Microbiology Spectrum. 2015;3(4):1-45. DOI: 10.1128/microbiolspec.MB-0018-2015
31.Bellon-Fontaine MN, Rault J, Van Oss CJ. Microbial adhesion to solvents: A novel method to determine the electron-donor/electron-acceptor or Lewis acid-base properties of microbial cells. Colloids and Surfaces. B, Biointerfaces. 1996;7(1-2):47-53. DOI: 10.1016/0927-7765(96)01272-6
33.Zhao X, Zhao F, Wang J, Zhong N. Biofilm formation and control strategies of foodborne pathogens: Food safety perspectives. RSC Advances. 2017;7(58):36670-36683. DOI: 10.1039/C7RA02497E
34.Takahashi H, Suda T, Tanaka Y, Kimura B. Cellular hydrophobicity of Listeria monocytogenes involves initial attachment and biofilm formation on the surface of polyvinyl chloride. Letters in Applied Microbiology. 2010;50(6):618-625. DOI: 10.1111/j.1472-765X.2010.02842.x
36.Mohana Sheela G, Prathyusha AMVN, Neelapu NRR, Bramhachari PV. Intra and inter-species communication in microbes: Living with complex and sociable neighbors. In: Bramhachari PV, editor. Implication of Quorum Sensing System in Biofilm Formation and Virulence. Singapore: Springer; 2018. pp. 7-16. DOI: 10.1007/978-981-13-2429-1
37.Liu L, Zeng X, Zheng J, Zou Y, Qiu S, Dai Y. AHL-mediated quorum sensing to regulate bacterial substance and energy metabolism: A review. Microbiological Research. 2022;262:127102. DOI: 10.1016/j.micres.2022.127102
38.Diggle SP, Crusz SA, Cámara M. Quorum sensing. Current Biology. 2007;17(21):R907-R910. DOI: 10.1016/j.cub.2007.08.045
39.Suppiger A, Schmid N, Aguilar C, Pessi G, Eberl L. Two quorum sensing systems control biofilm formation and virulence in members of the Burkholderia cepacia complex. Virulence. 2013;4(5):400-409. DOI: 10.4161/viru.25338
40.Dsouza FP, Dinesh S, Sharma S. Understanding the intricacies of microbial biofilm formation and its endurance in chronic infections: A key to advancing biofilm-targeted therapeutic strategies. Archives of Microbiology. 2024;206(2):85. DOI: 10.1007/s00203-023-03802-7
41.Kreve S, Dos Reis AC. Effect of surface properties of ceramic materials on bacterial adhesion: A systematic review. Journal of Esthetic and Restorative Dentistry. 2022;34(3):461-472. DOI: 10.1111/jerd.12799J
42.Muruzović MŽ, Mladenović KG, Čomić LR. In vitro evaluation of resistance to environmental stress by planktonic and biofilm form of lactic acid bacteria isolated from traditionally made cheese from Serbia. Food Bioscience. 2018;23:54-59. DOI: 10.1016/j.fbio.2018.03.005
43.Dygico LK, Gahan CG, Grogan H, Burgess CM. The ability of Listeria monocytogenes to form biofilm on surfaces relevant to the mushroom production environment. International Journal of Food Microbiology. 2020;317:108385. DOI: 10.1016/j.ijfoodmicro.2019.108385
44.Chaieb K, Chehab O, Zmantar T, Rouabhia M, Mahdouani K, Bakhrouf A. In vitro effect of pH and ethanol on biofilm formation by clinical ica-positive Staphylococcus epidermidis strains. Annales de Microbiologie. 2007;57:431-437. DOI: 10.1007/BF03175085
45.Biswas T, Ahmed M, Mondal S. Mixed species biofilm: Structure, challenge and its intricate involvement in hospital associated infections. Microbial Pathogenesis. 2024;195:106866. DOI: 10.1016/j.micpath.2024.106866
46.Al-Amshawee S, Yunus MYBM, Lynam JG, Lee WH, Dai F, Dakhil IH. Roughness and wettability of biofilm carriers: A systematic review. Environmental Technology and Innovation. 2020;21:101233. DOI: 10.1016/j.eti.2020.101233
47.Delolme C, Spadini L, Muris M, Causse B, Gaudet JP. Comparison of the acid–base reactivity of free-living Pseudomonas putida cells and biofilm. Chemical Geology. 2011;289(1-2):48-54. DOI: 10.1016/j.chemgeo.2011.07.007
48.Chen Y, Harapanahalli AK, Busscher HJ, Norde W, van der Mei HC. Nanoscale cell wall deformation impacts long-range bacterial adhesion forces on surfaces. Applied and Environmental Microbiology. 2014;80(2):637-643. DOI: 10.1128/AEM.02745-13
49.Cherif-Antar A, Moussa–Boudjemâa B, Didouh N, Medjahdi K, Mayo B, Flórez AB. Diversity and biofilm-forming capability of bacteria recovered from stainless steel pipes of a milk-processing dairy plant. Dairy Science and Technology. 2016;96:27-38. DOI: 10.1007/s13594-015-0235-4
50.Di Ciccio P, Vergara A, Festino AR, Paludi D, Zanardi E, Ghidini S, et al. Biofilm formation by Staphylococcus aureus on food contact surfaces: Relationship with temperature and cell surface hydrophobicity. Food Control. 2015;50:930-936. DOI: 10.1016/j.foodcont.2014.10.048
51.Zore A, Bezek K, Jevšnik M, Abram A, Runko V, Slišković I, et al. Bacterial adhesion rate on food grade ceramics and Teflon as kitchen worktop surfaces. International Journal of Food Microbiology. 2020;332:108764. DOI: 10.1016/j.ijfoodmicro.2020.10876
52.Teixeira P, Lopes Z, Azeredo J, Oliveira R, Vieira MJ. Physico-chemical surface characterization of a bacterial population isolated from a milking machine. Food Microbiology. 2005;22(2-3):247-251. DOI: 10.1016/j.fm.2004.03.010
53.Mishra A, Aggarwal A, Khan F. Medical device-associated infections caused by biofilm-forming microbial pathogens and controlling strategies. Antibiotics. 2024;13(7):623. DOI: 10.3390/antibiotics13070623
54.Teo AJ, Mishra A, Park I, Kim YJ, Park WT, Yoon YJ. Polymeric biomaterials for medical implants and devices. ACS Biomaterials Science & Engineering. 2016;2(4):454-472. DOI: 10.1021/acsbiomaterials.5b00429
55.Crawford RJ, Webb HK, Truong VK, Hasan J, Ivanova EP. Surface topographical factors influencing bacterial attachment. Advances in Colloid and Interface Science. 2012;179:142-149. DOI: 10.1016/j.cis.2012.06.015
56.Paxton NC, Allenby MC, Lewis PM, Woodruff MA. Biomedical applications of polyethylene. European Polymer Journal. 2019;118:412-428. DOI: 10.1016/j.eurpolymj.2019.05.037
57.Kasemo B. Biological surface science. Surface Science. 2002;500(1-3):656-677. DOI: 10.1016/S0039-6028(01)01809-X
59.Artham T, Sudhakar M, Venkatesan R, Nair CM, Murty KVGK, Doble M. Biofouling and stability of synthetic polymers in sea water. International Biodeterioration & Biodegradation. 2009;63(7):884-890. DOI: 10.1016/j.ibiod.2009.03.003
60.Arnold JW, Bailey GW. Surface finishes on stainless steel reduce bacterial attachment and early biofilm formation: Scanning electron and atomic force microscopy study. Poultry Science. 2000;79(12):1839-1845. DOI: 10.1093/ps/79.12.1839
61.Banerjee I, Pangule RC, Kane RS. Antifouling coatings: Recent developments in the design of surfaces that prevent fouling by proteins, bacteria, and marine organisms. Advanced Materials. 2011;23(6):690-718. DOI: 10.1002/adma.201001215
62.Abebe GM. The role of bacterial biofilm in antibiotic resistance and food contamination. International Journal of Microbiology. 2020;2020(1):1-10. DOI: 10.1155/2020/1705814
63.Boulangé-Petermann L, Rault J, Bellon-Fontaine MN. Adhesion of Streptococcus thermophilus to stainless steel with different surface topography and roughness. Biofouling. 1997;11(3):201-216. DOI: 10.1080/08927019709378331
64.Bos R, Van der Mei HC, Busscher HJ. Physico-chemistry of initial microbial adhesive interactions–its mechanisms and methods for study. FEMS Microbiology Reviews. 1999;23(2):179-230. DOI: 10.1111/j.1574-6976.1999.tb00396.x
65.Babiak I, Pędzisz P, Janowicz J, Małdyk P. Antimicrobial biomaterials in the prevention and local treatment of infection in orthopedics. Chirurgia Narzadów Ruchu i Ortopedia Polska. 2018;83(6):221-228. DOI: 10.31139/chnriop.2018.83.6.44
66.Chen F, Boylan D, Khan FZ, Shan L, Monga D, Zimmern PE, et al. Patterning bacterial cells on quasi-liquid surfaces for biofilm morphological control. Advanced Functional Materials. 2024;34:2407099. DOI: 10.1002/adfm.202407099
67.Ciofu O, Moser C, Jensen PØ, Høiby N. Tolerance and resistance of microbial biofilms. Nature Reviews. Microbiology. 2022;20(10):621-635. DOI: 10.1038/s41579-022-00682-4
68.Cascioferro S, Carbone D, Parrino B, Pecoraro C, Giovannetti E, Cirrincione G, et al. Therapeutic strategies to counteract antibiotic resistance in MRSA biofilm-associated infections. ChemMedChem. 2021;16(1):65-80. DOI: 10.1002/cmdc.202000677
69.Alves P, Moreira JM, Miranda JM, Mergulhão FJ. Analysing the initial bacterial adhesion to evaluate the performance of antifouling surfaces. Antibiotics. 2020;9(7):421. DOI: 10.3390/antibiotics9070421
70.Cagnola GN, Cabrera JN, Negri RM, D’Accorso NB, Lizarraga L, Pettinari MJ. Biofilm formation of two different marine bacteria on modified PDMS surfaces is affected by surface roughness and topography. Current Microbiology. 2023;80(8):256. DOI: 10.1007/s00284-023-03370-5
71.Da Costa D, Exbrayat-Héritier C, Rambaud B, Megy S, Terreux R, Verrier B, et al. Surface charge modulation of rifampicin-loaded PLA nanoparticles to improve antibiotic delivery in Staphylococcus aureus biofilms. Journal of Nanbiotechnology. 2021;19:1-17. DOI: 10.1186/s12951-020-00760-w
Written By
Tugba Kilic
Submitted: 11 December 2024Reviewed: 27 December 2024Published: 21 January 2025
Open access peer-reviewed chapter
