Open access peer-reviewed chapter - ONLINE FIRST

Antifouling Strategies-Interference with Bacterial Adhesion

Written By

Zhen Jia

Submitted: January 20th, 2022 Reviewed: January 31st, 2022 Published: March 4th, 2022

DOI: 10.5772/intechopen.102965

IntechOpen
Bacterial Biofilms Edited by Theerthankar Das

From the Edited Volume

Bacterial Biofilms [Working Title]

Dr. Theerthankar Das

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Abstract

Biofilm refers to a viable bacterial community wrapped in self-produced extracellular polymeric substances (EPS) matrix. As bacteria shielded by EPS are viable and can resist broad hostile environments and antimicrobial agents, biofilm poses a massive challenge to industries and human health. Currently, biofilm has accounted for widespread and severe safety issues, infections, and economic loss. Various antifouling strategies have been designed and developed to prevent biofilm formation. As bacterial biofilm is perceived as a dynamic multistage process in which bacterial attachment on solid surfaces is the prerequisite for biofilm formation, the interference with the attachment is the most promising environmentally benign option to antifouling. The chapter summarizes and discusses the antifouling strategies that interfere with the adhesion between bacteria and substrate surfaces. These strategies primarily focus on modifying the substrate surface’s topographical and physicochemical properties.

Keywords

  • biofilm
  • antifouling
  • modification
  • topography
  • physicochemical property

1. Introduction

Bacterial biofilm is a structured community of bacterial cells within a self-generated hydrated extracellular polymetric substance (EPS) matrix anchored to a surface [1]. The physical channels formed during biofilm formation facilitate nutrients, air, and water to penetrate and distribute to cells [2], promoting microbial reproduction, metabolism, and EPS secretion. EPS is a biopolymer produced by bacterial cells following surface attachment, serving as a house or shelter for cells [3, 4]. It mainly consists of a wide variety of exopolysaccharides (40–95%), proteins (1–60%), nucleic acids (1–10%), and lipids (1–40%) [2, 5], which are critical factors to enhance bacterial adhesion behavior. On the one hand, EPS possesses mechanical stability, protecting cells from mechanical damages and shear and providing a functional microenvironment for bacterial growth [6]. On the other hand, EPS creates a physical barrier that enables bacteria inside to survive under harsh conditions and to resist antibiotics and antimicrobial agents [7].

Biofilm, different from planktonic cells, is a self-protection growth pattern of bacteria. Over 99% of the world’s bacteria present as a form of biofilm [8], broadly distributing on broad infrastructure elements, systems, and devices. Due to strong self-protection ability and resistance to harsh conditions, the unwanted biofilms pose severe threats and challenges to human health and industries, such as the transmissions of disease and infections and interferences of system functions and decreases in the endurance of surfaces and devices [9]. In the medical system, bacteria can form biofilm in healthcare settings (such as sinks, drains, and showers) and medical devices (such as surgical instruments and implantable biomedical devices). Up to 80% of hospital-acquired infections (HAIs) contribute to biofilm infections [10]. Such HAIs affect about 10% of all hospital patients in the United States and lead to nearly 100,000 deaths annually [11, 12]. In the food industry, biofilms have been widely reported on food surfaces, food contact surfaces, and processing systems, leading to product contamination, cross-contamination, food withdrawal, and disease outbreaks [13, 14, 15]. In the marine system, biofilm accumulation accelerates corrosion on marine vehicles, resulting in equipment clogging, damage, and roughness [16]. In addition, biofilm increases hydrodynamic drag, which adversely interferes with equipment performance and increases fuel expenditure up to 45% [17]. The economic losses caused due to biofilm are also enormous. For US Navy alone, the estimated fuel cost per annum is around $500 million, of which $75–100 million account for drag induced by fouling organisms [18]. Therefore, it is critical and urgent to prevent biofilm formation.

Biofilm formation is a dynamic process, typically containing five stages: initial reversible attachment, irreversible attachment, micro-colony formation, biofilm formation and maturation, and dispersion. Among them, initial reversible attachment is critical. In this stage, bacteria actively seek and anchor to surfaces relying on the motility of planktonic cells using extracellular organelles and proteins (such as pili, curli fibers, flagella, and outer membrane proteins), cells’ gravitational transportation, physical forces between cells and surfaces (such as van der Waals forces, steric interactions, and electrostatic interactions), and hydrodynamic forces of the surrounding environment [19, 20]. Additionally, other forces include acid-base interactions at a very short range, around 5 nm range, responsible for bond formation and hydrophobic forces [21] and divalent cations responsible for crosslinking between bacterial surface polymers that aid in matrix stabilization [22]. The attachment of a microbial cell to a surface is called adhesion [23]. The adhesion is reversible as bacteria are loosely attached. The attached cells still exhibit Brownian motion and can easily dissociate back to planktonic forms. The adhesion of bacteria is primarily influenced by various factors, including surface properties, environmental conditions (like pressure and temperature), and bacterial orientation [24].

Based on the process of biofilm formation, it is worth noting that bacterial adhesion is an initial prerequisite for biofilm formation. After being attached to surfaces, bacterial cells initiate to reproduce and ultimately grow into a biofilm, demonstrating that bacterial adhesion is the fundamental and critical step responsible for biofilm formation. Therefore, inhibiting bacterial adhesion is the desirable and key antifouling approach to prevent biofilm formation. The adhesion of bacteria is mainly affected by various factors, including surface properties of substrates, physicochemical properties of microbes, and environmental conditions [25]. As the properties of substrate surfaces are changeable and can be manipulated depending on the purpose, antifouling approaches to control biofilm formation mostly focus on modifying surface properties, including surface topography and physicochemistry (Table 1).

StrategiesPropertiesCoating
Physicochemical modificationHydrophilic surfacePolymers: PEO, PEG, OEG, poly-HEMA, dextran, phosphatidylcholines, poly (acrylic acid), etc.
Nanoparticles: TiO2, SiO2, ZnO, Fe3O4, silver nanoparticles, etc.
Hydrophobic surfaceSilicone-based coatings
Fluorine-based coatings
Sol-gel
Biosurfactants: surfactin & pseudofactin
Organic materials: polydimethylsiloxane, polyethylene, polystyrene, polyalkylpyrrole, etc.
Inorganic materials: ZnO and TiO2 etc.
Chemical propertiesMetal ions and their compounds: Zn, ZnO, Cu, CuO, Mg, MgO, TiO2, etc.
Biomacromolecules: proteins/peptides, polysaccharides, antibodies, etc.
Topographic modificationMicro-scale topography
Nano-scale topography

Table 1.

Surface modification techniques.

The purpose of this chapter is to provide insights into antifouling strategies related to the topographical and physicochemical properties of substrate surfaces in the prevention of cell adhesion and to elucidate corresponding theoretical mechanisms. This chapter also covers the main challenges and future trends of antifouling materials.

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2. Physicochemical modification strategy

It is well documented that bacterial adhesion can be effectively tuned and reduced by altering surface physicochemical properties using chemically active antifouling coatings [26, 27]. Currently, various coatings have been extensively reported for their effectiveness in preventing bacterial initial adhesion.

2.1 Surface energy

Surface energy is the binding or interfacial attractive force between materials and solid substrates [28]. It is an essential physicochemical property of a solid surface. Many studies have demonstrated that changing surface energy was related to affecting bacterial adhesion [29, 30]. Baier analyzed the relationship between surface energy and bacterial adhesion, known as the Baier curve depicted in Figure 1 [31]. According to the curve, bacterial adhesion is minimized when the surface energy of a substrate is in the range of 20–30 mN/m (the lowest values), while antifouling occurs when surface energy is higher than 70 mN/m [32, 33].

Figure 1.

Correlation between bacterial adhesion and surface energy (Baier curve).

Surface energy represents the degree to which water can bind on the surface [34] and can be determined by contact angle (θ) [35]. θcharacterizes the ability of water to maintain contact with a solid surface. ‘Hydrophilic surface (θ< 90°)’ and ‘hydrophobic surface (θ≥ 90°)’ are two common terms to describe the incongruous behavior of water on solid surfaces [36]. Hydrophilic surfaces are surfaces with high surface energy, while hydrophobic surfaces are surfaces with low surface energy [37].

2.1.1 Hydrophilic surfaces

Hydrophilic surfaces can be successfully fabricated by functionalizing with polymers or nanoparticles. Polymers include poly (ethylene oxide) (PEO), poly (ethylene glycol) (PEG), oligo (ethylene glycol) (OEG), dextran, phosphatidylcholines, poly (acrylic acid), and poly-(2-hydroxyethyl methacrylate) (poly-HEMA), etc. [38]. Nanoparticles cover TiO2, SiO2, ZnO, Fe3O4, and silver nanoparticles [39, 40, 41, 42]. The presence of ▬CH2▬ CH2▬O▬ structure and C▬C▬C linkage enable PEG to be highly water-soluble [43].

Many researchers have reported the antiadhesion ability of hydrophilic surfaces. An increase in surface hydrophilicity can reduce bacterial adhesion [44]. Dong et al. indicated that PEG-modified SS exhibited higher hydrophilicity than bare stainless steel (SS), leading to a 96% reduction in Listeria monocytogenesattachment [45]. ZnO nanoparticles, composed of hydrophilic groups like ▬OH, ▬SO3H, and ▬COOH, possess strong hydrophilicity [46]. The increased hydrophilicity derived from ZnO nanoparticles promoted antifouling properties of poly (ether sulfone) surface towards Escherichia coli(E. coli) and Staphylococcus aureus(S. aureus) [47].

Superhydrophilic surfaces hold near-zero water contact angles (θ < 5°) and exhibit outstanding antifouling properties. Superhydrophilic surfaces can be developed by hydrophilic functionalities, such as metal oxides including TiO2, ZnO, SiO2, SnO2, CuO, and WO3, by applying various fabrication methods (e. g. UV irradiation, plasma, sol-gel self-assembly, etching, and spay/spin/dip-coating) [48, 49, 50]. TiO2 and ZnO are the primary metal oxides to create superhydrophilic film due to their photoinduced self-cleaning property [51, 52]. SiO2 is also frequently used due to its low price and easy to reach [53]. The adhesion number of E. colicells on superhydrophilic TiO2 coated surface was approximately 45% lower than the surface without coating [54]. Qian et al. prepared superhydrophilic film on the 316L stainless steel surface using methoxy-polyethylene-glycol thiol [55]. The surface showed excellent superhydrophilicity with a water contact angle of zero and exhibited enhanced and more durable antibacterial performances against E. coliand S. aureus[55].

The antiadhesion mechanism of the (super)hydrophilic surface contributes to forming a highly hydrated layer. Hydrophilic compounds on substrate surfaces, such as PEG or OEG, can strongly bond water molecules, connecting each chain through ether oxygen and generating a thin water film (a highly hydrated layer) between bacteria and surface, which physically blocks bacterial adhesion (as shown in Figure 2A) [56, 57]. In addition, the number of anchor sites can be effectively diminished by the water layer [58]. The more hydrophilic surface is, the more resistant it is to the adhesion of bacteria [59].

Figure 2.

Mechanism of superhydrophilic (A) and superhydrophobic (B) surfaces.

2.1.2 Hydrophobic surfaces

Hydrophobic coatings, such as silicone- or fluorine-based coatings, polydimethylsiloxane (PDMS), and sol-gel, enable the surface to be more hydrophobic [60]. Besides, some biosurfactants, like surfactin secreted by genus Bacillusstrains and pseudofactin produced by Pseudomonas fluorescens, have also been verified to successfully promote surface hydrophobicity [61, 62]. Extensive studies demonstrated that hydrophobicity was closely associated with the antiadhesive ability of surfaces. The adhesion-resistant ability of hydrophobic surfaces is attributed to low surface energy. Microbial adhesion is less to low-energy surfaces and more accessible to clean because of weaker binding at the interface [63]. Zhao et al. compared bacterial adhesion behavior on hydrophobic surfaces with various surface energy, indicating that the number of E. coliattachments was significantly reduced when surface energy ranged between 20 and 30 mJ/m2 [64]. By spraying hydrophobic perfluoroalkoxy/nano-silver coatings onto aluminum substrates, Zhai et al. found that besides contact killing of silver ions, the hydrophobic surface property could synergistically prevent the adhesion of E. coli[65]. With the presence of surfactin coating (surface energy is roughly 27 mN/m), stainless steel, polypropylene, and polyvinyl chloride could effectively prohibit adhesion of Enterobacter sakazakii, Listeria monocytogenes(L. monocytogenes), and SalmonellaTyphimurium [66, 67].

A superhydrophobic surface is a surface having a water contact angle greater than 150°, a sliding grade lower than 5°, and high stability of the Cassie model state [68, 69]. In general, superhydrophobic surfaces can be acquired by rendering with fluorocarbon materials containing -CF3 and ▬CF2▬ groups, silicones, organic materials (for example, polyethylene, polystyrene, and polyalkylpyrrole), and inorganic materials (like ZnO and TiO2) [68, 70, 71, 72]. The remarkable and well-known property of superhydrophobic surfaces is that an air layer known as air plastron is physically entrapped between liquid and surface (as shown in Figure 2B) when a substrate is immersed in liquid or bacterial suspension [73]. The air plastron exhibits a great potency in antifouling and corrosive resistance [74]. The contact area between bacteria and the superhydrophobic surface is reduced by the air plastron, resulting in significant mitigation of adherent bacteria [74, 75]. In addition, due to the higher contact angle and low sliding angle of a superhydrophobic surface, droplets cannot stay on the superhydrophobic surface and roll off immediately, known as the ‘lotus effect,’ accounting for the low-adhesion or self-cleaning property of the superhydrophobic surface [76, 77]. An approximately 80% reduction in the adhesion of E. coliK-12 was achieved on a superhydrophobic surface [54]. Freschauf et al. demonstrated low initial concentration (~2%) of E. colicould attach to the superhydrophobic polystyrene, polycarbonate, and polyethylene surfaces [78]. Compared to bare glass, poly-pyrene-F6 coated glass showed a significant impact against bacterial attachment: bacterial adhesion could be diminished by about 65% for Pseudomonas aeruginosa(P. aeruginosa) and S. aureus[79].

2.2 Chemical properties

2.2.1 Metal ions and their compounds

Metals in various forms, coated on substrate surfaces, are well known for their antibacterial effects [80, 81]. The main metals applied include silver, gold, copper, zinc, magnesium, calcium, cerium, strontium, nickel, titanium, europium, yttrium ions, and anions (such as selenium and fluoride) [82]. Silver can deactivate protein activities by interacting with thiol groups in proteins and interfere with transmembrane energy generation and ion transport by generating stable S-Ag bonds in the cell membrane [81]. Moreover, the silver ion can bind to nucleic acid, affecting replication ability and denaturing them [81, 83]. The antibacterial capability of silver has been utilized to prevent bacterial infection for decades, and nearly 650 types of bacteria are associated [84, 85]. Copper exhibits contact-killing properties by damaging cell membranes, inducing the formation of reactive oxygen species (ROS), inhibiting enzymes’ activities, and denaturing nucleic acid [81]. Estimated 90 types of bacteria have been reported to be killed using contacting copper [81]. In hospitals, copper alloys, used in doorknobs and other surfaces, exerted an antimicrobial effect against E. coliO157, methicillin-resistant S. aureus(MRSA), and Clostridium difficilewhile equivalent stainless-steel surfaces did not [86].

Metal oxides such as zinc oxide (ZnO), copper oxide (CuO), Fe2O3, MgO, and titanium oxide (TiO2) have been implemented to prevent biofilm formation in recent years since they are stable under harsh conditions and generally safe for humans and animals [87]. Among metal oxide antibacterial agents, ZnO and TiO2 aroused increasing attention due to their efficient antibacterial activities on a broad spectrum of bacteria [88, 89]. The antibacterial ability of ZnO may contribute to its destruction of bacterial cell integrity and the formation of ROS [90]. ZnO is a photocatalytic material that can respond to UV light and induce ROS creation [91]. TiO2, also known as a photocatalyst, has received more attention because of its strong antiadhesion and antibacterial properties [92]. Moreover, TiO2 is abundant in nature, biologically and chemically stable, non-toxic, corrosion-resistive, and inexpensive [93]. When illuminated by ultraviolet light with paper energy under aerobic conditions, TiO2 can induce the generation of electrons and holes that react with organic substance and dioxygen molecules to form hydroxyl radicals and superoxide ions, preventing bacteria from adhering to substrate surfaces [94, 95, 96] by penetrating cell walls, rupturing membrane, and discomposing organic substances [97, 98]. Many studies have reported TiO2-coated surfaces exhibited antiadhesion properties against both Gram-negative and Gram-positive bacteria, such as S. aureusand Streptococcus mutants[99], E. coli[93], L. monocytogenes[100], and Salmonella[101].

Besides, metal/metal oxide nanoparticles and metal-organic frameworks (MOFs) are porous materials with nanostructures, acting as reservoirs of metal ions. They also possessed significant antibacterial ability, inhibiting biofilm formation and acting as antiadhesion agents [102]. The mechanisms of their actions are similar to those at the molecular level [103].

2.2.2 Biomacromolecules

Surfaces modified by natural/synthetic proteins/peptides exhibit effective ability to prevent/reduce bacterial adhesion [104]. Proteins/peptides are low toxicity, assembly, and biocompatibility and can be coated on the surfaces of various materials, such as metals, oxides, and polymers [105]. Proteins/peptides avoid bacterial attachment by shifting the hydrophobicity of surfaces and providing hydration [106]. Binding between proteins and bacterial cells is also responsible for adhesion resistance [107]. In addition, due to zwitterionic charges and high hydrogen bond-donor/acceptor abilities of polar functional groups, proteins can interact with negative charged groups on the bacterial cell membrane, destructing cells’ integrity [108, 109, 110] and exhibiting non-fouling characteristics [111]. Albumins, such as human serum albumin (HSA) and bovine serum albumin, are remarkable proteins that can prevent bacterial adherence to implant surfaces. Eighty-two to ninety-five percent of S. aureuswas significantly inhibited from binding to HAS-coated titanium surfaces [112]. The antibody is a ‘Y-shaped’ protein. Its opsonization can impede the adhesion of bacterial cells to implant surfaces by blocking the way of cell-surface attachment and phagocytizing cells [113]. With the presence of antibodies, the adhesion of E. coliwas markedly reduced on polymer substrates [114].

Probiotic microorganisms, such as Lactobacillusand Lactic acid bacteria (LAB), play an important role in antiadhesion. Due to their high adherence capability, probiotics exhibited vigorous antiadhesion activity by competing with bacteria for attachment sites [115]. In addition, antimicrobial substances (such as bacteriocins and hydrogen peroxide) produced by probiotics can also inhibit bacterial adhesion [116]. Studies on the antiadhesion ability of LAB and Lactobacillusstrains have been largely reported, including Lactobacillus fermentum (L. fermentum)in the prevent adhesion of S. aureus[117], antiadhesion effects of L. Plantarum, L. crustorum, L. coryniformis, and L. rhamnosuson E. coli[118], and antiadhesion activity of L. crispatusagainst Enterococcus faecalis[115].

Bioactive materials present effective possibilities of resisting biofilm formation. Polysaccharides are a crucial bioactive substance [119], like chitosan, hyaluronic, and alginic acid. The mechanism of the antiadhesion capability of polysaccharides might be that polysaccharides could dissolve biofilms by interacting with the EPS layer and distort biofilm formation and kill cells by inhibiting the metabolic activity of bacterial cells [120]. Chitosan possesses significant antibacterial and antibiofilm activities, making it widely used in medical and food fields, such as food preservation, scaffolds, and bandages [121, 122, 123]. The positive-charge property of chitosan enables it to bind with negatively charged cell membranes, inducing the leakage of proteinaceous and other intracellular constituents [124]. Moreover, chitosan can cross through the membrane, bind with DNA, and interfere with the synthesis of mRNA and protein [113]. It was found that chitosan with quaternary ammonium groups could eradicate biofilm formation of Staphylococcus aureus[125], and carboxymethyl chitosan could restrain S. aureusor P. aeruginosafrom adhering to surfaces with an efficiency of >90% [126].

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3. Topographic modification strategy

Topographical features of substratum surfaces can modulate bacterial attachment and biofilm formation as surface morphology dominates surface roughness and wettability [127]. Typically, the topographical surface can be classified into three different scales: macro-, micro-, and nano-scale [128]. Roughness is a critical factor affecting bacterial attachment by reducing the attachment area between a particle and a surface [129]. Since most microbes are approximately 0.2–2 μm in diameter [130] which is much smaller than the groove distance of macro-roughness, cells can swim and entrap into the grooves of macro-roughness surfaces, suggesting that macro-scale roughness surfaces are not related to antifouling [127]. Therefore, micro-and nano-scale topography surfaces are crucial for preventing bacterial adhesion. Many studies have investigated how micro/nano-scale topographies affect bacterial adhesion. Discrete, ordered, and hierarchical surface structures from nano-scale to micro-scale were self-assembled, designed, or bioinspired by mimicking natural surfaces (such as skins of marine mammals and sharks, shells of mollusks and crabs, wings of insects and birds, and leaves of plants) [131, 132].

3.1 Micro-scale topography surfaces

Micro-structure can be fabricated on surfaces of metals, plastics, and polymer films, like stainless steel [133], polyethylene terephthalate (PET) [134], and PDMS [135]. The micro-patterned topographies exhibited positive influences on preventing the adhesion of various bacteria strains while being non-toxic [135]. Wang et al. designed and fabricated micro-patterned PET surfaces, which simultaneously include curved and straight edges, flat plateaus (top of pillars), and flat surfaces between pillars [134]. The results indicated that PET surfaces with pillars could significantly reduce the attachment of E. colicells under both static and dynamic (shaking at 200 r/min) conditions in nutritious media and oligotrophic solution at 37°C. The Sharklet diamond-shaped micropattern, inspired by shark surface architecture, was widely reported due to its impressive ability to prevent colonization and biofilm formation of various bacteria strains, including Mycobacterium abscessus[136], E. coli[137], S. aureus[138], and P. aeruginosa[139].

Features of micropatterns, including pattern shape, size, and groove distance, affect antifouling efficiency [140]. Varied topographical pattern shapes have been created and presented antiadhesion ability. Pattern shapes cover ordered geometric shapes (i.e. line [26], pyramid [141], and cross [142]), pillar [143], pit [144], brush [145], wrinkle [17], and biomimetic shapes (like Sharklet diamond shape [136], lotus-like shape [146], rice leaf [147], rose petals [148], and mytilid shells [149]). In general, with the increase in pattern size, the antiadhesion ability of micropatterns decreased. Lu et al. studied the adhesion of E. coli, P. aeruginosa, and S. aureuson micro-patterned PDMS films with three different pattern sizes [135]. It was found that when pattern size was smaller than bacteria size, the surface was effective in preventing bacteria adhesion; however, as the pattern size was comparable to or larger than bacteria size, the antiadhesion capability of the surface decreased markedly, with more bacteria attachment but still less compared with the flat surface. Similar results were reported by other researchers [150]. This phenomenon might be attributed to the contact area between microorganisms and the surfaces. The available cell-surface contact area reduces with a smaller pattern size than bacterial cell size [151]. The groove between patterns provides anchor sites for cell contact, creates vortices under dynamic conditions, and acts as dead zones for cells sheltered from sanitation treatment [152, 153]. It was also reported that bacteria prefer to distribute in the grooves rather than the top of protruding patterns [135]. As groove distance is smaller than bacteria size, less bacterial cells are entrapped [154]. Similar results were obtained by Lu et al. and Romero et al. [135, 155]. However, the attachment of bacteria can be enhanced when the groove distance is equal to bacteria size because microorganism cells can fit between grooves, and binding energy can be increased [135].

Besides, the effectiveness of surface microstructures on antifouling is also affected by surface energy and hydrophobicity [156]. According to Wenzel and Cassie and Baxter, surface topography can alter the surface to be hydrophobic and superhydrophobic [157]. Carman et al. demonstrated that hexagons could increase the hydrophobicity of the polydimethylsiloxane elastomer [158]. Micro-scale structure could enhance surface hydrophobic ability, allowing more air bubbles to effectively form between surface and liquid [159]. Since a large portion of surfaces was occupied by air, the contact area between bacteria and surfaces was significantly reduced, leading to less cell attachment [160]. Additionally, due to the effect of surface tension, bacteria cannot cross the air-water interface, thereby inhibiting bacterial adhesion [157].

3.2 Nano-scale topography surfaces

Nano-topography provides an effective way to repel bacterial adhesion and prohibit biofouling. Like the micro-scale patterns, the topographical features such as shape, size, density, and groove width can markedly affect cell adhesion onto surfaces [161, 162]. Compared to low-density patterns, nanostructures with highly dense patterns greatly improve the reduction rate of bacterial attachment [163, 164]. Adhesion numbers of E. coliand S. aureuswere significantly reduced by 55.6 and 40.5% on a nanoscale (6 nm) titanium surface with a low density of 213 peaks/μm2 compared to 2 nm with a high density of 2240 peaks/μm2 [165].

Numerous shapes of nano-patterns with varying size, depth, and groove width have been reported as excellent impeders of bacterial adhesion and biofilm formation [166, 167, 168, 169]. A topographical surface characterized by nanometer-size pores (approximately 0.20 μm2) surrounded by nano ridges, mimicking the pilot whale skin, exhibited antifouling activity based on reduced available space for bacterial attachment [170]. The more the topography resembled the size and shape of features on bio-skins, the better the antifouling activity was [16, 171]. Bhadra et al. fabricated a nanowire array (average size is approximately 40.2 nm) on titanium and estimated its antifouling ability [172]. It was revealed that the nanowire arrays could render titanium as a moderately effective bactericidal surface, with more excellent bactericidal activity, eliminating almost 50% of P. aeruginosacells and about 20% of S. aureuscells. The surfaces of cicada and dragonfly wings exhibit bactericidal properties towards some bacteria strains due to their nano-scale pillar structure [173, 174]. Cicada-inspired fluoridated hydroxyapatite with nanopillars has been successfully fabricated using electrochemical additive manufacturing (ECAM) by Ge et al. [175]. Different types of nanopillar array were obtained: with diameters, heights, and aspect ratios of ~65–95 nm, ~380–510 nm, and ~4.5–7.5 nm, respectively. It was demonstrated that the nanopillars with diameters of ~80 nm were lethal to both Gram-negative and Gram-positive bacteria when the nanopillar density is proper [176, 177].

The cell-nanostructure adhesion mechanisms are still poorly understood. Currently, there are three mechanisms proposed to elucidate the antifouling behavior of nano-textured surfaces. (1) nanostructures induce the formation of the superhydrophobic surface [178]. As explained by the Cassie-Baxter state, the nanostructure can promote air pockets generating in the solid/liquid interface and increase the surface contact angle [179]. As a result, the available contact area for bacteria on the surface is reduced, thus preventing bacterial adhesion [180]. (2) Bacterial membrane can be ruptured and stretched by the nanostructure, leading to cell disruption and eventually cell death, known as the biophysical model, developed by Pogodin et al. [181]. This occurs because the size of most bacterial cells is in the micrometer range, while the structured surfaces are in the nanometer range [182]. Based on the model, bacterial cells absorbed on pattern surface may lead to a drastic increase of contact area, accompanied by stretching the cell membrane between the pillars, which induces membrane disruption and cell death. Furthermore, in terms of the model, the rigidity of cell membranes plays a crucial role in bacterial attachment behavior: the more rigid cells are, the more resistant they are. This may be the reason why nano-pillared surfaces were less effective against gram-positive bacteria strains (Bacillus subtilis, Planococcus maritimus, and S. aureus) when compared to less rigid gram-negative bacteria strains (P. aeruginosa) [173, 183, 184, 185]. (3) Since the nano-structured topography is unfavorable for bacterial cells, the immobilized cells push and pull the structure while attempting to move away, imposing fatal shear force on the membrane, which initiates bacterial membrane damage [174]. In addition, the solid adhesive force between bacteria and nanostructure also facilitates membrane deformation and cell membrane rupture [174].

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4. Conclusions, challenges, and future trends

Bacterial biofilm is a universal and ubiquitous phenomenon. It can directly cause severe problems on public health, the environment, and industries and subsequently lead to economic losses. Consequently, various strategies have been developed and implemented to control biofilm formation. As bacterial adhesion on a surface is the prerequisite for biofilm formation, much attention has been paid to the antifouling strategies that utilize topography and physicochemistry modification to prevent bacterial adhesion to surfaces. This chapter only summarizes the positive effect of surface topographical and physicochemical properties on preventing bacterial adhesion. However, inconsistent and even conflicting impacts could be found in various reported studies. No one particular surface structure or physicochemical property has demonstrated universal antiadhesion ability against all types of microorganisms. Therefore, it is needed to continue the development of strategies that are truly and broadly effective. Furthermore, though surface topographical and physicochemical properties exhibited significant and effective ability to resist the adhesion of specific bacteria strains, the surface structures and physicochemical properties are easily destroyed by various forces, thus decreasing their antifouling capabilities. Therefore, developing a long-term and durable surface with effective antifouling properties remains a huge challenge for the future.

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Zhen Jia

Submitted: January 20th, 2022 Reviewed: January 31st, 2022 Published: March 4th, 2022