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.
KeywordsMedical adhesives Wet adhesion Bio-inspiration Coacervation
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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- Watts DC. Chapter II.5.8 - Adhesives and Sealants. In: Hoffman AS, Schoen FJ, Lemons JE, editors. Biomaterials Science (Third Edition): An Introduction to Materials in Medicine. 3rd Edition. Oxford: Elsevier; 2013. p. 889–904.Google Scholar
- Wei W, Petrone L, Tan Y, Cai H, Israelachvili JN, Miserez A, Waite JH. An underwater surface-drying peptide inspired by a mussel adhesive protein. Adv Funct Mater. 2016;26:3496–507.View ArticleGoogle Scholar
- Seo S, Lee DW, Ahn JS, Cunha K, Filippidi E, Ju SW, Shin E, Kim B-S, Levine ZA, Lins RD, Israelachvili JN, Waite JH, Valentine MT, Shea JE, Ahn BK. Significant performance enhancement of polymer resins by bioinspired dynamic bonding. Adv Mater. 2017; 10.1002/adma.201703026.
- Maier GP, Rapp MV, Waite JH, Israeachvili JN, Butler A. Adaptive synergy between catechol and lysine promotes wet adhesion by surface salt displacement. Science. 2015;349:628–31.View ArticleGoogle Scholar
- Rapp MV, Maier GP, Dobbs HA, Hingdon NJ, Waite JH, Butler A, Israelachvili JN. Defining the Catechol-cation synergy for enhanced wet adhesion to mineral surfaces. J Am Chem Soc. 2016;138:9013–6.View ArticleGoogle Scholar
- Priemel T, Degtyar E, Dean MN, Harrington MJ. Rapid self-assembly of complex biomolecular architectures during mussel byssus biofabrication. Nat Commun. 2016;8:14539.View ArticleGoogle Scholar
- Cowin SC. Bone Mechanics Handbook. New York: CRC Press; 2001.Google Scholar
- Kuehn K-D, Ege W, Gopp U. Acrylic bone cements: composition and properties. Orthop Clin North Am. 2005;36:17–28.View ArticleGoogle Scholar
- Dunne N, W. R. MWCNT Used in Orthopaedic Bone Cements. In: Naraghi DMBT-CN-G and A, editor. Carbon Nanotubes - Growth and Applications. Rijeka: InTech; 2011. p. Ch. 14. doi:10.5772/20317.
- Vertebroplasty & Kyphoplasty. https://www.mayfieldclinic.com/PE-Kyphoplasty.htm. Accessed 28 June 2017.
- Mathis JM, Barr JD, Belkoff SM, Barr MS, Jensen ME, Deramond H. Percutaneous vertebroplasty: a developing standard of care for vertebral compression fractures. Am J Neuroradiol. 2001;22:373–81.Google Scholar
- Dental adhesive. https://www.ivoclarvivadent.us/mam/celum/celum_assets/8937274376222_Adhese_Universal_pdf_5800.pdf?3. Accessed 28 June 2017.
- Pelletier MH, Lau AC, Smitham PJ, Nielsen G, Walsh WR. Pore distribution and material properties of bone cement cured at different temperatures. Acta Biomater. 2010;6:886–91.View ArticleGoogle Scholar
- Webb J, Spencer R. The role of polymethylmethacrylate bone cement in modern orthopaedic surgery. Bone Joint J. 2007;89:851–7.View ArticleGoogle Scholar
- Harrigan T, Kareh J, O'Connor D, Burke D, Harris W. A finite element study of the initiation of failure of fixation in cemented femoral total hip components. J Orthop Res. 1992;10:134–44.View ArticleGoogle Scholar
- Miller MD, Thompson SR, Hart J. Review of orthopaedics: Elsevier health sciences; 2012.Google Scholar
- Smith D. Medical and dental applications of cements. J Biomed Mater Res A. 1971;5:189–205.View ArticleGoogle Scholar
- Smith DC. Development of glass-ionomer cement systems. Biomaterials. 1998;19:467–78.View ArticleGoogle Scholar
- Das S, Lee BH, Linstadt RT, Cunha K, Li Y, Kaufman Y, Levine ZA, Lipshutz BH, Lins RD, Shea J-E. Molecularly smooth self-assembled monolayer for high-mobility organic field-effect transistors. Nano Lett. 2016;16:6709–15.View ArticleGoogle Scholar
- Dupraz A, Meer SV, Wijn J, Goedemoed J. Biocompatibility screening of silane-treated hydroxyapatite powders, for use as filler in resorbable composites. J Mater Sci Mater Med. 1996;7:731–8.View ArticleGoogle Scholar
- Lee JH, Um CM, Lee IB. Rheological properties of resin composites according to variations in monomer and filler composition. Dent Mater. 2006;22:515–26.View ArticleGoogle Scholar
- Gooding JJ, Ciampi S. The molecular level modification of surfaces: from self-assembled monolayers to complex molecular assemblies. Chem Soc Rev. 2011;40:2704–18.View ArticleGoogle Scholar
- Ikada Y. Tissue adhesives: Wound closure biomaterials and devices. Boston: CRC Press; 1997.Google Scholar
- Bioglue cardiac surgery. http://www.levibio.it/en/levibio-tech-en/bioglue-specialita-cardiochirurgia.html. Accessed 28 June 2017.
- Medical adhesive. https://www.linkedin.com/pulse/medical-adhesive-market-outlook-global-trends-forecast-sindhu-k. Accessed 28 June 2017.
- Andrews GP, Laverty TP, Jones DS. Mucoadhesive polymeric platforms for controlled drug delivery. Eur J Pharm Biopharm. 2009;71:505–18.View ArticleGoogle Scholar
- Karp JM, Langer R. Materials science: dry solution to a sticky problem. Nature. 2011;477:42–3.View ArticleGoogle Scholar
- Geim AK, Dubonos S, Grigorieva I, Novoselov K, Zhukov A, Shapoval SY. Microfabricated adhesive mimicking gecko foot-hair. Nat Mater. 2003;2:461–3.View ArticleGoogle Scholar
- Lee H, Lee BP, Messersmith PB. A reversible wet/dry adhesive inspired by mussels and geckos. Nature. 2007;448:338–41.View ArticleGoogle Scholar
- Hollinsky C, Kolbe T, Walter I, Joachim A, Sandberg S, Koch T, Rülicke T. Comparison of a new self-gripping mesh with other fixation methods for laparoscopic hernia repair in a rat model. J Am Coll Surg. 2009;208:1107–14.View ArticleGoogle Scholar
- Lee BP, Messersmith PB, Israelachvili JN, Waite JH. Mussel-inspired adhesives and coatings. Annu Rev Mater Res. 2011;41:99–132.View ArticleGoogle Scholar
- Comyn J. The relationship between joint durability and water diffusion, Developments in Adhesives - Part2. London: Applied Science Publishers; 1981.Google Scholar
- Pocius AV. Adhesion and Adhesives Technology. Ohio: Hanser Pub; 1997.Google Scholar
- Silverman HG, Roberto FF. Understanding marine mussel adhesion. Mar Biotechnol. 2007;9:661–81.View ArticleGoogle Scholar
- Mattila J. The importance of shelter, disturbance and prey interactions for predation rates of tube-building polychaetes (Pygospio Elegans (Claparede)) and free-living tubificid oligochaetes. J Exp Mar Biol Ecol. 1997;218:215–28.View ArticleGoogle Scholar
- Miserez A, Li Y, Cagnon J, Weaver JC, Waite JH. Four-stranded coiled-coil elastic protein in the byssus of the giant clam, Tridacna maxima. Biomacromolecules. 2012;13:332–41.View ArticleGoogle Scholar
- Kamino K. Mini-review: barnacle adhesives and adhesion. Biofouling. 2013;29:735–49.View ArticleGoogle Scholar
- Wei W, Tan Y, Rodriguez NRM, Yu J, Israelachvili JN, Waite JH. A mussel-derived one component adhesive coacervate. Acta Biomater. 2014;10:1663–70.View ArticleGoogle Scholar
- Wilker JJ. Biomaterials: Redox and adhesion on the rocks. Nat Chem Biol. 2011;7:579–80.View ArticleGoogle Scholar
- Stewart RJ, Ransom TC, Hlady V. Natural underwater adhesives. J Polym Sci B Polym Phys. 2011;49:757–71.View ArticleGoogle Scholar
- Faure E, Falentin-Daudré C, Jérôme C, Lyskawa J, Fournier D, Woisel P, Detrembleur C. Catechols as versatile platforms in polymer chemistry. Prog Polym Sci. 2013;38:236–70.View ArticleGoogle Scholar
- Martinez Rodriguez NR, Das S, Kaufman Y, Israelachvili JN, Waite JH. Interfacial pH during mussel adhesive plaque formation. Biofouling. 2015;31:221–7.View ArticleGoogle Scholar
- Yu J, Wei W, Danner E, Ashley RK, Israelachvili JN, Waite JH. Mussel protein adhesion depends on interprotein thiol-mediated redox modulation. Nat Chem Biol. 2011;7:588–90.View ArticleGoogle Scholar
- Ortony JH, Hwang DS, Franck JM, Waite JH, Han S. Asymmetric collapse in biomimetic complex coacervates revealed by local polymer and water dynamics. Biomacromolecules. 2013;14:1395–402.View ArticleGoogle Scholar
- Mussel-inspired adhesives – Messersmith Research Group. https://bioinspiredmaterials.berkeley.edu/research/mussel-inspired-adhesives/. Accessed 28 June 2017.
- Brubaker CE, Kissler H, Wang L-J, Kaufman DB, Messersmith PB. Biological performance of mussel-inspired adhesive in extrahepatic islet transplantation. Biomaterials. 2010;31:420–7.View ArticleGoogle Scholar
- Li Y, Meng H, Liu Y, Narkar A, Lee BP. Gelatin microgel incorporated poly (ethylene glycol)-based bioadhesive with enhanced adhesive property and bioactivity. ACS Appl Mater Interfaces. 2016;8:11980–9.View ArticleGoogle Scholar
- Skelton S, Bostwick M, O'Connor K, Konst S, Casey S, Lee BP. Biomimetic adhesive containing nanocomposite hydrogel with enhanced materials properties. Soft Matter. 2013;9:3825–33.View ArticleGoogle Scholar
- Liu Y, Lee BP. Recovery property of double-network hydrogel containing a mussel-inspired adhesive moiety and nano-silicate. J Mater Chem B. 2016;4:6534–40.View ArticleGoogle Scholar
- Liu Y, Meng H, Qian Z, Fan N, Choi W, Zhao F, Lee BP. A moldable Nanocomposite Hydrogel composed of a mussel-inspired polymer and a Nanosilicate as a fit-to-shape tissue sealant. Angew Chem Int Edit. 2017;56:4224–8.View ArticleGoogle Scholar
- Development of applied biomaterials – Bruce Lee Research Group. http://bplee.biomed.mtu.edu/research/. Accessed 28 June 2017.
- Seo S, Das S, Zalicki PJ, Mirshafian R, Eisenbach CD, Israelachvili JN, Waite JH, Ahn BK. Microphase behavior and enhanced wet-cohesion of synthetic copolyampholytes inspired by a mussel foot protein. J Am Chem Soc. 2015;137:9214–7.View ArticleGoogle Scholar
- Ahn BK. Perspectives on mussel-inspired wet adhesion. J Am Chem Soc. 2017;139:10166–71.Google Scholar
- Ahn BK, Das S, Linstadt R, Kaufman Y, Martinez-Rodriguez NR, Mirshafian R, Kesselman E, Talmon Y, Lipshutz BH, Israelachvili JN. High-performance mussel-inspired adhesives of reduced complexity. Nat Commun. 2015;6:8663.View ArticleGoogle Scholar
- Studying sea life for a glue that mends people. http://www.nytimes.com/2010/04/13/science/13adhesive.html. Accessed 28 June 2017.
- Endrizzi BJ, Stewart RJ. Glueomics: an expression survey of the adhesive gland of the sandcastle worm. J Adhes. 2009;85:546–59.View ArticleGoogle Scholar
- Chollakup R, Beck JB, Dirnberger K, Tirrell M, Eisenbach CD. Polyelectrolyte molecular weight and salt effects on the phase behavior and coacervation of aqueous solutions of poly (acrylic acid) sodium salt and poly (allylamine) hydrochloride. Macromolecules. 2013;46:2376–90.View ArticleGoogle Scholar
- Priftis D, Xia X, Margossian KO, Perry SL, Leon L, Qin J, de Pablo JJ, Tirrell M. Ternary, tunable polyelectrolyte complex fluids driven by complex coacervation. Macromolecules. 2014;47:3076–85.View ArticleGoogle Scholar
- Srivastava S, Andreev M, Levi AE, Goldfeld DJ, Mao J, Heller WT, Prabhu VM, de Pablo JJ, Tirrell MV. Gel phase formation in dilute triblock copolyelectrolyte complexes. Nat Commun. 2017;8:14131.View ArticleGoogle Scholar
- Stevens MJ, Steren RE, Hlady V, Stewart RJ. Multiscale structure of the underwater adhesive of Phragmatopoma Californica: a nanostructured latex with a steep microporosity gradient. Langmuir. 2007;23:5045–9.View ArticleGoogle Scholar
- Medical adhesives – Russell Stewart Research Group. http://www.bioen.utah.edu/faculty/RJS/LabSite12/medical%20adhesives.html. Accessed 28 June 2017.
- Zhao H, Sun C, Stewart RJ, Waite JH. Cement proteins of the tube-building polychaete Phragmatopoma Californica. J Biol Chem. 2005;280:42938–44.View ArticleGoogle Scholar
- Zhao Q, Lee DW, Ahn BK, Seo S, Kaufman Y, Israelachvili JN, Waite JH. Underwater contact adhesion and microarchitecture in polyelectrolyte complexes actuated by solvent exchange. Nat Mater. 2016;15:407–12.View ArticleGoogle Scholar
- Stewart RJ, Wang CS, Shao H. Complex coacervates as a foundation for synthetic underwater adhesives. Adv Colloid Interf Sci. 2011;167:85–93.View ArticleGoogle Scholar
- Stunkard HW. Life histories and systematics of parasitic worms. Syst Zool. 1953;2:7–18.View ArticleGoogle Scholar
- Hammond RA. The proboscis mechanism of Acanthocephalus Ranae. J Exp Biol. 1966;45:203–13.Google Scholar
- Verweyen L, Klimpel S, Palm HW. Molecular phylogeny of the Acanthocephala (class Palaecanthocephala) with a paraphyletic assemblage of the orger Polymorphida and Echinorhynchida. PLoS One. 2011;6:e28285.View ArticleGoogle Scholar
- Yang SY, O’Cearbhaill ED, Sisk GC, Park KM, Cho WK, Villiger M, Bouma BE, Pomahac B, Karp JM. A bio-inspired swellable microneedle adhesive for mechanical interlocking with tissue. Nat Commun. 2013;4:1702.View ArticleGoogle Scholar
- Seong K-Y, Seo M-S, Hwang DY, O’Cearbhaill ED, Sreenan S, Karp JM, Yang SY. A self-adherent, bullet-shaped microneedle patch for controlled transdermal delivery of insulin. J Control Release. 2017:doi.org/10.1016/j.jconrel.2017.03.041.