Advances in medical adhesives inspired by aquatic organisms’ adhesion
© The Author(s). 2017
Received: 18 July 2017
Accepted: 11 September 2017
Published: 10 October 2017
In biomedicine, adhesives for hard and soft tissues are crucial for various clinical purposes. However, compared with that under dry conditions, adhesion performance in the presence of water or moisture is dramatically reduced. In this review, representative types of medical adhesives and the challenging aspects of wet adhesion are introduced. The adhesion mechanisms of marine mussels, sandcastle worms, and endoparasitic worms are described, and stemming from the insights gained, designs based on the chemistry of molecules like catechol and on coacervation and mechanical interlocking platforms are introduced in the viewpoint of translating these natural adhesion mechanisms into synthetic approaches.
The high industrial and biomedical demands for adhesives have led to major progresses in the discovery of their molecular mechanisms as well as the development of the surface science and engineering of adhesive materials. In particular, the advances in polymer science and the usage of lightweight materials have been driven by the aerospace and automobile industries . Whereas, the strict requirements (e.g., biocompatibility, toxicity, and strong adhesive performance) of biomedical adhesives have limited the development of wide-ranging products. For example, the performance of adhesives is dramatically reduced underwater or moisturized conditions. For this reason, researchers have endeavored to improve adhesion efficiency in the presence of water or moisture (termed “wet adhesion”). Moreover, medical adhesives require strong wet adhesion at multifaceted physiological conditions (e.g., pH, salts, and biological molecules).
To overcome these challenges of strong wet adhesion, researchers have been interested in how aquatic organisms survive by attachment/adherence underwater or on wet surfaces. With progresses in understanding the mechanisms and key elements of the natural adhesion observed in aquatic organisms, medical adhesives have been developed via mimicking the adhesion procedures or utilizing the crucial functional groups. The most investigated study is to develop synthetic adhesives inspired by marine mussels [2–6]. They used chemical moieties, e.g., catechols (an analog of the Dopa group of adhesive mussel foot proteins) for tailoring synthetic adhesives. In addition, unique formulation of coacervation (critical step in the formation of the protein-based underwater adhesives) were utilized for constructing efficient wet adhesives.
The aim of this review is to give a brief introduction of various medical adhesives and the challenging aspects of wet adhesion. This review will cover three examples of aquatic organisms’ adhesion – marine mussels, sandcastle worms, and endoparasitic worms, and their insights that can be translated to synthetic platforms and an overview of current synthetic adhesives for biomedical applications.
An effective adhesive requires appropriate materials and adhesion techniques corresponding to diverse biomedical circumstances (host environments), because biological hosts respond differently to the adhesives used for hard or soft tissues.
Hard tissue adhesives
Poly(methyl methacrylate) (PMMA) has been extensively used for bone cements because the acrylic cement hardens to ~90% of its final mechanical properties within a short time (13–18 min) , enabling load bearing and offering immediate stability. However, PMMA-based bone cements have two major limitations. First, PMMA does not have intrinsic adhesive properties, and only acts as a space filler to closely hold the implant against the bone . Such a weak interfacial link between the cement and bone (or implant) results in implant failure . Second, PMMA is a brittle, notch-sensitive material. Although its Young’s modulus (~2 GPa) is 1–2 times higher than that of the surrounding cancellous bone, it is still ~100 times lower than that of the metal prosthesis . Thus, the interspatial bone cement needs to be a shock-buffering spacing between an inflexible bone and a hard implant .
Tooth cements (Fig. 1b) have been used for various dental applications, such as a luting agent or for protecting pulps from injury. They help in sealing or fixing and casting the filling substance to both the dentin and enamel. Most of these materials are hard and/or brittle because the load-bearing polymer composites include metallic or ceramic fillers that are hardened by an acid–base reaction  or polymerization .
Additionally, dental primers have been applied as a way of priming a tooth surface and simultaneously enhancing the adhesion or bonding of the bulk resin composites. For the priming of inorganic fillers, such as silicate minerals, silane-based primers are most commonly used. However, the silane grafting chemistry uses potentially toxic chemicals [19, 20] and tough processing [21, 22] and, therefore, there is a great demand for alternative dental primers.
Soft tissue adhesives
Soft tissue adhesives are generally planned to be used for transitory or short-term purposes, where they can be removed or degraded when wound healing has progressed sufficiently. For integration of the adhesive with soft tissues that are surrounded by wet tissue fluid or blood, the adhesive needs to be spread easily on the surface and show effective wet adhesion in an adequate working time .
The most common examples of soft tissue adhesives are bioglues or sealants  (Fig. 1c) and patches  (Fig. 1d). Bioglues are usually applied as surgical adhesives in cardiovascular, neurological, and soft tissue surgeries. One such example, BioGlue (Levi BioTECH), was demonstrated to lessen bleeding during cardiac procedures (e.g., aortic dissection, and replacement and implantation of biomedical devices).
In particular, mucosal tissues are required for protection against external and harmful stimuli as well as for treatment with controlled drug delivery. Mucosal adhesives are polymer-based drug delivery platforms, where the degree of cross-linking, the chain length, and the presence of various functional groups in the polymer determine the degree of adhesive bonding and the successful control of drug delivery to the target sites .
Patch-type adhesives are also currently used in the clinical field owing to their advantages, including reduced operation times and enhanced tissue handling in a large area. In particular, a glue-coated patch is commonly used as a conventional skin adhesive. However, owing to the allergic reactions and skin irradiation encountered with use of conventional skin adhesives, the fabrication of such types of adhesives without chemical methods is required . Introducing micro- or nanostructures onto the surface of patches has been proven to increase soft tissue adhesion with minimal tissue irritation. Inspired by gecko feet, Geim et al.  demonstrated enhanced adhesion using micropatterned poly(imide) films prepared by photolithography and dry etching techniques. The adhesive strength was related to the number of polyimide microstructures present. However, the adhesive performance of the microfabricated patches diminished when submerged in a moist environment, such as bloody tissue or sweaty skin, because of decreased intermolecular interactions. To overcome this limitation, nanofabricated pillar arrays coated with mussel-inspired polymeric glue have been developed . The poly(dimethylsiloxane) nanopillar films coated with poly(dopamine methacrylamide-co-methoxyethyl acrylate) showed reversible adhesion under both dry and wet conditions. Tissue adhesion is highly affected by the chemical and physical properties of the tissue surface. Since tissues have a surface roughness in the range of a few microns to a few millimeters, it is difficult to form a high level of adhesion when the two surfaces of the tissues are not in contact. To achieve universal tissue adhesion regardless of surface conditions, mechanical interlocking-based adhesion is advantageous. Mesh-type adhesion patches with club-shaped hooks have been shown to provide strong adherence to the internal organs of hernias, via entanglement with the tissue surface . In addition, if the hook is made of a biodegradable polymer, it can be easily removed after a certain period of time.
The water in most cells and tissues consist of ~70% by weight as the medium. Additionally, cells, tissues, and implants are typically surrounded by saline water (e.g., blood plasma, lymph, etc.). In the viewpoint of biomedical adhesion, the medium unfortunately creates limited durable binding between the host biological system and the medical adhesive , because the water or moisture acts as a surface contaminant or weak boundary layer at the bond interface. This reduced adhesion performance in the presence of water or moisture occurs with most synthetic adhesives. The weakened performance is known to be influenced by complex reasons, such as the hydrolysis of polymers, moisture-induced plasticization, swelling, and erosion .
Adhesion mechanisms of aquatic organisms and their inspired medical adhesives developments
For aquatic organisms, attachment (or adherence) is a survival strategy in tough water environments [34, 35]. For example, marine mussels/giant clams and barnacles adhere to rock surfaces by using their byssus and secreted cement proteins, respectively [34, 36]. Aquatic larvae and black fly pupae anchor to environmental surfaces using adhesive proteins . Here, unique motifs (viz., the coacervate formation/platform, and mechanical interlocking mechanism) will be discussed with respect to their role in the natural adhesion.
The interface between a marine mussel’s byssal adhesive plaque and a glass substrate resembles a porous-like structure but with pillar-shaped attachment  (Fig. 3e). Such structure and shape at the interface can be considered promising architectures for the design of underwater adhesives.
As an example of such catechol-functionalized polymers, polyethylene glycol (PEG)-catechol adhesives have been studied in biomedical applications, where the adhesion performance and interfacial progress (i.e., tissue biocompatibility, and integrity of the tissue and the adhesive) were investigated in mice . After implantation of the polymeric adhesives, no noticeable inflammatory cell infiltrates and fibrotic capsule formation appeared at the given time  (Fig. 4b, left). After several months, vascularization was well structured on the implant site of the catechol polymer-immobilized islets  (Fig. 4b, right). Thus, the PEG-catechol adhesives demonstrated biocompatibility in biomedical applications and appropriate integrity toward the host tissue. Likewise, Lee’s group focused on developing tissue adhesives with tunable physical, mechanical, and adhesive properties that combined high strength with the ability to support tissue ingrowth and wound healing [47–51] (Fig. 4c). Additionally, the Waite and Kollbe group considered other constitutional features of interfacial Mfps, such as cationic residues (lysine, K), anionic residues (aspartic acid, D), nonionic polar residues (asparagine, N), and nonpolar residues (alanine, A), to create mussel-inspired synthetic wet-adhesion systems [19, 52–54] (Fig. 4d and e).
One good example of such adhesive platforms using complex coacervation is the synthetic polyelectrolytes established by the Stewart group [57, 60], which mimic the polyelectrolytic proteins in the sandcastle glue  (Fig. 5d). Those authors were inspired by the dense, phase-separated fluid of the sandcastle glue-like polyelectrolytic proteins. They formed various supramolecular platforms—from colloidal structures to insoluble precipitates or ionic gels—and optimized them into sandcastle glue-mimicking coacervates by controlling the solution conditions and polymer structures. For condensation of the polyelectrolytes, an entropic driving force was employed; such as electrostatic charge neutralization between the polymeric charges to displace small counterions and water.
The Waite group also developed concrete underwater constructs inspired by the sandcastle worm’s glue-like protein mortar . This worm uses a significant principle for the design of such structures by selecting sand granular particles with a protein mortar glues  (Fig. 5e, left). Upon deposition onto the particle surfaces, the coacervate becomes three-dimensional porous solid structure regarded as by incorporation of the coacervates and structural maturation of the metal ion- protein complexes. Based on cross-links by oxidized l-Dopa, the tubular walls were then cured [39, 63, 64] (Fig. 5e, right).
In the development of medical adhesives, wet adhesion is an inherent and considerable point of challenge. Through bioinspired or biomimetic ways of translating natural adhesion mechanisms into synthetic approaches, it is possible to save the time-consuming synthesis of adhesives. As reviewed herein, translation of the natural adhesion mechanisms of the marine mussel, sandcastle worm, and endoparasitic worms into synthetic platforms—ranging from synthetic molecules and colloidal systems to coacervation and mechanical interlocking processes—will help to realize the design and fabrication of effective underwater adhesives for biomedical applications.
This work was supported by a 2-Year Research Grant of Pusan National University (201708040001).
2-Year Research Grant (Pusan National University, 201,708,040,001).
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