Supramolecular Adhesive Materials with Antimicrobial Activity: Comparison
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Taking advantage of the dynamic and reversible interactions such as hydrogen bonding, pi-pi stacking, electrostatic interactions, host-guest interactions, hydrophobic effects, and van der Waals interactions, a variety of functional supramolecular adhesive materials have been developed to realize tough bonding on tissues or organs. Non-covalent interactions are widely exploited and proved effective in developing supramolecular polymers and polymer composites with desired mechanical strength, interfacial adhesion, and intelligent, responsive properties. These supramolecular adhesive materials are promising for a range of biomedical applications.

  • adhesive materials
  • antimicrobial activity
  • biomedical applications

1. The Features of Adhesive Materials in the Biomedical Field

Adhesive materials have provided great value as alternatives or adjuncts for sutures, clips, staples, and other commercial bio-glues. In recent years, many sophisticated adhesive materials have employed versatile interfacial interactions such as chemical anchors and non-covalent interactions to bind with tissues or organs for the diagnosis and treatment of diseases (Table 1) [1][2][3][4]. These noninvasive strategies promote the development of on-demand adhesion properties in biological systems, making adhesive materials customized for a range of scenarios.
Table 1. Mechanisms of the adhesive materials for bonding the biological tissues or organs.
Adhesion Mechanism on Biological Tissues or Organs
Type Adhesive Bond Topological Connection
Chemical Anchor Non-Covalent Bond Topological Interlocking Physical Entanglement Mechanical Interlock
Pro (s) High bonding energy with biological tissues or organs; Available under complex physiological environment (e.g., blood, interstitial fluid) Temporary and reversible bonding with biological tissues or organs; Interfacial interactions (e.g., hydrogen bonding, charge interaction) can be controlled by molecular designs Adhesion properties (e.g., bonding energy, reversibility) can be controlled by the molecular or structural designs; Stimuli-responsive bonding behaviors (e.g., pH, temperature) can be realized; Available under complex physiological environment (e.g., blood, interstitial fluid)
Con (s) Permanent and irreversible bonding with biological tissues or organs Low bonding energy with wet biological tissues or organs; Easy of debonding under complex physiological environment (e.g., blood, interstitial fluid) Require complex and time-consuming processing on the surfaces of tissues or organs; Unavailable on smooth and nonporous surfaces of tissues or organs
Bioactive polymers with various functions such as hemostasis and sealing are often used to prepare the adhesives for applications in biological systems. Although most adhesives derived from natural polymers have low immunogenicity, which may not induce adverse reactions during the use period, some derivatives from the biopolymers, such as the quaternized chitosan and biogenic collagen, still present poor biocompatibility. Because tissues are mainly composed of water-containing liquid and various proteins such as the glycoproteins in cell membranes and collagens, they will carry abundant functional hydrophilic groups originating from the amino acids [5]. The use of chitosan can improve the wet adhesion ability with the tissue surfaces due to the hydrophilic interactions. In addition, the amino groups of chitosan can be protonated into -NH3+ for antimicrobial activity, as well as the recruitment of the red blood cells to assist the formation of clots for blood coagulation, providing a suitable hemostatic effect. Introducing more quaternary ammonium groups on the backbone of chitosan can increase the number of cationic centers, but a large number of quaternization will cause increased toxicity to surrounding cells and tissues. Collagen is another welcomed natural polymer for preparing biofunctional adhesives, as it can activate the platelet adhesion and the following expression of coagulation factors VIII, IX, XI, and XII [6]. As a hydrolysis product from collagen, gelatin can also retain the main biofunctions for the adhesives.
Compared with natural polymers, synthetic polymers can be endowed with advantages that may be weaknesses in natural polymers. For example, surface adhesion, cell behaviors, and biofunctions are all controllable by rational molecular design and material engineering methods. Polyethylene glycol (PEG) is a widely used synthetic polymer for adhesives since it provides intrinsic adhesiveness to tissues and has suitable physiological compatibility. Furthermore, its molecular structure can be engineered with additional groups (e.g., dopamine, aldehyde group) to promote adhesion properties or transformed into hyperbranched morphologies for more available functional groups [7]. For example, ureidopyrimidinone (UPy)-functionalized PEG hydrogel has shown fast, precise, and local drug-releasing and self-healing abilities. The non-covalent interactions between the UPy motifs made the hydrogel injectable ascribed to the shear-thinning behaviors. The combined pH-responsive drug release, self-healing, and injectable properties enabled the PEG-based hydrogel as the minimally invasive material to induce the generation of growth factors for treating myocardial infarction [8]. However, the realization of all the demanded properties, either by natural polymers or synthetic polymers, is tough due to the conflicts in the molecular or structural designs. It is essential to orchestrate the properties that are required in different biomedical applications, which raises huge demand for the combination of chemistry, material, and biological expertise.
Based on the abundant non-covalent interactions and topological connections of the polymer network, adhesive materials prepared by supramolecular interactions show a series of advantages over traditional commercial and covalently crosslinked adhesives, including tunable mechanical properties, tough and reversible adhesion performance, rapid self-healing ability, suitable cargo-loading capacity, and different functions. These properties can be grouped or tuned through unique supramolecular designs to satisfy the application requirements in diverse biological systems. Monofunctional or multifunctional adhesive materials can be obtained accordingly, and one or multiple properties could be focused in response to the complicated requirements of biological systems. In the following, various adhesive materials’ designs will be analyzed to interpret the potential in emerging biomedical applications.

2. Supramolecular Adhesive Materials with Antimicrobial Activity

Pathogen transmissions occur everywhere, from public facilities and medical settings to the human body and biomedical implants [9]. Once the pathogens are colonized onto the implants and medical devices in the nosocomial environment, severe safety problems such as infections and other complications would occur to the patients. Once biofilms are formed, much more effort is required because biofilms are much more difficult to destroy than planktonic bacteria, which are not protected by the extracellular polymeric substances (EPS) [10]. Therefore, adhesive materials with a prominent antimicrobial function will extend their application scope. The antimicrobial capability in the adhesives is usually originated from the endogenous or exogenous antimicrobial components, which can help prevent the transmission of pathogens such as bacteria, fungi, and viruses. The antimicrobial adhesives applied in the biological systems also provide infection prevention, which is an important protection for the host during surgical operations. These adhesive materials can be divided into three categories according to their action mechanisms in killing pathogens: biocide-releasing, contact-killing, and stimuli-responsive killing.

2.1. Design Adhesive Materials for Release-Killing

Supramolecular polymers, particularly the supramolecular gels, show high loading ratios for a wide range of biocides, such as antibiotics [11][12][13], metal nanoparticles [14][15][16], nitrogen oxide [17][18][19], and essential oils [20][21][22][23]. Due to the weak interactions between the polymeric chains and antimicrobial agents, or the encapsulation of antimicrobial agents in the porous structures, the incorporated antimicrobial agents can be released from the supramolecular polymers into the aqueous medium in a well-controlled way to kill planktonic bacteria and biofilms [24][25]. Generally, the involved action mechanism is that antimicrobial agents interfere with the metabolism of pathogens. They can damage the cell membranes, suppress protein activity, and inhibit nucleic acid replication [25]. Metal nanoparticles such as silver nanoparticles are often incorporated into the supramolecular polymers as a wound dressing due to the broad-spectrum antimicrobial activity and low bio-toxicity to the human body [26]. For example, one type of antimicrobial adhesive, Gel-TA, made from oxidized tannic acid and gelatin, was used to crosslink with the silver nitrate [27]. The Gel-TA adhesives showed excellent cytocompatibility and pronounced wet adhesion properties on the tissues through mussel-inspired adhesion chemistry and outstanding antimicrobial activities to bacteria and fungi, resulting from the inherent antimicrobial capacity of tannic acid and silver nanoparticles. However, the used antimicrobial metal nanoparticles in a high dose would present some toxicity to the human body [28]. Antibiotics such as gentamicin, tobramycin, ampicillin, vancomycin, and minocycline are commonly loaded into the adhesives. For example, Hu et al. reported an injectable hydrogel co-loaded with the antibiotic amikacin and anti-inflammatory naproxen [29]. This hydrogel showed a couple of combinational properties, including stimuli-responsive releasing behaviors, mechanical integrity, suitable biocompatibility, antimicrobial activity, and anti-inflammation response.
Although antibiotics still play an important role in controlling pathogens’ proliferation, abusing antibiotics could accelerate the resistance to drugs [24][25][30]. To avoid the resistance caused by the abuse of antibiotics, environmentally friendly antimicrobial strategies have been developed. Essential oils derived from plants have been considered green antimicrobial agents due to their suitable biocompatibility, low cost, and broad-spectrum antimicrobial ability [21][31]. TheOur group recently developed a carvacrol-regulated mucus-inspired adhesive through crosslinking intermolecular hydrogen-bonded polyurea and carvacrol [20]. The obtained supramolecular adhesives exhibited suitable transparency, tunable mechanical properties, reusable adhesion behaviors, controlled release, and long-term antimicrobial activity. The content of incorporated carvacrol will cause many variations such as mechanical properties and release behaviors due to the various intensities of hydrogen bonding interactions between supramolecular polymers and essential oils. The adhesive might help address the issues of virus/pathogen-contained aerosols. ResearchWers then reported another mucus-inspired supramolecular organogel adhesive coating, which could effectively control the pathogen spread by respiratory microdroplets  [21]. In this supramolecular system, a polyurea scaffold could provide mechanical strength and accommodate different kinds of lubricant oils. The carvacrol could regulate the hydrogen-bonded network and provide antimicrobial functions, and the silicone oil endowed the organogels with self-healable and lubricant properties. The supramolecular organogel coating could adhere to the substrates and provide a wrapping-layer-assisted disinfection mechanism through the released carvacrol. The pathogen-containing microdroplets were spatially wrapped by the lubricant oils, which would increase the release rate of carvacrol for rapid disinfection. Although the biocide-releasing strategy has drawn wide attention and has been frequently used in antimicrobial adhesives, the limited content of antimicrobial agents could hinder the sustained activity of the adhesives, which may require frequent replacement of the adhesives for continuous disinfection [25].

2.2. Design Adhesive Materials for Contact-Killing

Adhesive materials with contact-killing properties can circumvent the limited content of incorporated antimicrobial agents. They realize the disinfection by contacting the surface of pathogens using their antimicrobial components. The effective antimicrobial moieties usually consist of polycations, antimicrobial peptides, and antimicrobial enzymes, which can covalently or non-covalently link to the polymeric chains [30][32]. The antimicrobial mechanisms of contact-killing are diversified, mainly including the cell membranes’ physical lysing or charge disruption [25]. However, the contact-active adhesives usually suffer because the bacteria within the infected tissues or protected by EPS may not come into contact with the antimicrobial components. Therefore, the adhesive should be able to release its components to penetrate the biofilms for disinfection. Gan et al. developed a tough supramolecular hydrogel adhesive by an interpenetrated polymeric network, which included terpolymers and quaternized chitosan [33]. The dual crosslinking (covalent and non-covalent) endowed the hydrogel with strong and tough mechanical properties. The monomer of methacrylamide dopamine enabled the hydrogel to contact and adhere to the fibroblasts. Moreover, the quaternized chitosan provided intrinsic antimicrobial abilities for supramolecular adhesives. Therefore, this type of contact-active supramolecular hydrogel could be used for tissue regeneration and wound disinfection. Although these cationic polymers exhibited effective antimicrobial activities, the toxicity to mammalian cells is still a concern that could not be ignored. Antimicrobial peptides (AMPs) are composed of cationic and amphiphilic molecules, which are considered an alternative with available antimicrobial activity and cytocompatibility [24][30][34][35]. A recently reported biomimetic surface engineering strategy integrated the mussel-inspired adhesive peptide with bio-orthogonal click chemistry [36]. The dibenzylcyclooctyne (DBCO)-modified AMPs and DBCO-modified nitric oxide generating species of 1,4,7,10-tetraazacyclododecane-1,4,7,10-tetraacetic acid (DOTA) chelated copper ions are clicked onto the surfaces for durable antimicrobial properties and ability in long-term resistance of adhesion/activation of platelets. The engineered surface can therefore be applied to many biomedical devices to prevent infection and thrombosis. In addition, it is reported that the antimicrobial capabilities of the peptide-based supramolecular hydrogels are primarily influenced by the side chain length, charge density, and amphiphilicity of the AMPs [24]

2.3. Design Adhesive Materials for Stimuli-Responsive Killing

External physical or chemical changes can activate stimuli-responsive antimicrobial properties of the adhesive materials. This type of adhesive material can usually generate hyperthermia or active molecules such as the reactive oxygen under the trigger by light, electricity, magnetism, and ultrasound [25][30][37]. Some adhesives could also be prepared with responsive abilities to environmental factors such as temperature, pH, and humidity [38][39][40]. The stimuli-responsive ability endows the adhesives with controllable antimicrobial activity that may reduce the development of pathogen resistance. Adhesives integrated with photothermal and photodynamic antimicrobial functions have shown prominent values in numerous biomedical applications. A wide range of nano-agents such as gold nanoparticles, carbon nanomaterials, and metal-sulfide nanomaterials have excellent light-to-heat conversion capacity [41][42][43][44], while the photosensitizers could also lead to the damage of membranes and DNA molecules of the pathogen [45].
Taking advantage of the UPy-assisted supramolecular interactions, reswearchers have developed one supramolecular nanocomposite adhesive coating [43]. The adhesive coating was mechanically induced by the assembly of powders, which contained the mixture of the siloxane-modified gold nanorods and siloxane-derived crosslinkers. The nanocomposite adhesive coatings exhibited fast preparation, strong adhesion, high stiffness, rapid disinfection ability, and remarkable disinfection effectiveness over 99.9% to different kinds of multi-drug-resistant bacteria within 6 s near-infrared irradiation (NIR). Liang et al. reported an antimicrobial adhesive hydrogel through a dual-dynamic-bond crosslinked mechanism consisting of ferric iron, protocatechualdehyde, and quaternized chitosan [44]. The dynamic properties of catechol-Fe coordination and Schiff base bonds endowed the adhesive with self-healing and on-demand dissolution or removal properties. The quaternized chitosan provided the inherent antimicrobial ability, and the compound of catechol-Fe with NIR properties provided the photo-responsive antimicrobial capability. Despite the photo-induced heating having made significant progress, the generated heat may also damage the local cells and tissues [25]. For adhesives with photodynamic antimicrobial function, the incorporated photosensitizers could transform the light energy into chemical energy to induce the generation of active molecules such as hydroxyl radicals, superoxide, or singlet oxygen for pathogen disinfection. For example, Castriciano et al. reported an antimicrobial scaffold with photosensitizer releasing ability. The scaffold was fabricated from the polypropylene fabrics and loaded with the poly (carboxylic acid)-cyclodextrin/anionic porphyrin through the typical host-guest interactions [46]. This method showed a sustained and efficient photodynamic antimicrobial activity to Gram-positive S. aureus and Gram-negative P. aeruginosa. Paul et al. also developed a light-activatable nanospray coating with photodynamic therapy of microbes [47]. The sustainable antimicrobial coating from adhesive, UV-resistant, and antimicrobial lignin-integrated abilities of photoluminescence and singlet oxygen generation render the coating promising in phototheranostic applications. Moreover, supramolecular polymers containing photosensitizers usually showed better antimicrobial activity to Gram-positive bacteria than Gram-negative bacteria due to the structural differences in the cell membranes [45][48]. These results demonstrated that the stimuli-responsive properties enabled the adhesive materials to have smart properties.

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