Advances in aquatic bio-inspired medical adhesives_Journal of Biomedical Engineering

Authors：

WU Yun ^1,2,3 ,  LI Jian ¹

1. Pharmacy, People's Liberation Army Southern Theater General Hospital, Guangzhou 510010, P.R.China;
2. College of Pharmacy, Guangdong Pharmaceutical University, Guangzhou 510006, P.R.China;
3. Pharmacy, University of Chinese Academy of Sciences Shenzhen Hospital, Shenzhen, Guangdong 518107, P.R.China;

Corresponding author：

Keywords：

medical adhesive; adhesion mechanism; underwater biology; tissue adhesion

DOI：

10.7507/1001-5515.201805051

Video：

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In recent years, due to the dramatic increase in the number of surgical operations, there has been a clinically significant increase in the demand for medical adhesives capable of cohesion in a moist environment that can overcome blood or tissue fluids in vivo. As the understanding of the mechanisms and key elements of natural adhesion to aquatic organisms continues to develop, a variety of medical adhesives have been developed by mimicking adhesion procedures or utilizing key functional groups. This article will review the classification, adhesion mechanism, use, research progress and development prospects of biomedical adhesives inspired by aquatic organisms octopus and mussels.

Citation： WU Yun, LI Jian. Advances in aquatic bio-inspired medical adhesives. Journal of Biomedical Engineering, 2019, 36(2): 325-333. doi: 10.7507/1001-5515.201805051 Copy

1.	Seo S, Lee D W, Ahn J S, et al. Significant performance enhancement of polymer resins by bioinspired dynamic bonding. Adv Mater, 2017, 29(39). DOI: 10.1002/adma.201703026.
2.	Priemel T, Degtyar E, Dean M N, et al. Rapid self-assembly of complex biomolecular architectures during mussel byssus biofabrication. Nat Commun, 2017, 8: 14539.
3.	Rapp M V, Maier G P, Dobbs H A, et al. Defining the catechol-cation synergy for enhanced wet adhesion to mineral surfaces. J Am Chem Soc, 2016, 138(29): 9013-9016.
4.	Zhao Yanhua, Wu Yang, Wang Liang, et al. Bio-inspired reversible underwater adhesive. Nat Commun, 2017, 8(1): 2218.
5.	Lee H, Um D S, Lee Y, et al. Octopus-inspired smart adhesive pads for transfer printing of semiconducting nanomembranes. Adv Mater, 2016, 28(34): 7457-7465.
6.	Chen Yingchu, Yang Hongta. Octopus-inspired assembly of nanosucker arrays for dry/wet adhesion. ACS Nano, 2017, 11(6): 5332-5338.
7.	Baik S, Kim D W, Park Y, et al. A wet-tolerant adhesive patch inspired by protuberances in suction cups of octopi. Nature, 2017, 546(7658): 396-400.
8.	Chen L, An H Z, Haghgooie R, et al. Flexible octopus-shaped hydrogel particles for specific cell capture. Small, 2016, 12(15): 2001-2008.
9.	Went P T, Lugli A, Meier S, et al. Frequent EpCam protein expression in human carcinomas. Hum Pathol, 2004, 35(1): 122-128.
10.	Dendukuri D, Pregibon D C, Collins J, et al. Continuous-flow lithography for high-throughput microparticle synthesis. Nat Mater, 2006, 5(5): 365-369.
11.	Dendukuri D, Gu S S, Pregibon D C, et al. Stop-flow lithography in a microfluidic device. Lab Chip, 2007, 7(7): 818-828.
12.	Björnmalm M, Yan Y, Caruso F. Engineering and evaluating drug delivery particles in microfluidic devices. J Control Release, 2014, 190: 139-149.
13.	Pregibon D C, Toner M, Doyle P S. Multifunctional encoded particles for high-throughput biomolecule analysis. Science, 2007, 315(5817): 1393-1396.
14.	Suh S K, Yuet K, Hwang D K, et al. Synthesis of nonspherical superparamagnetic particles: in situ coprecipitation of magnetic nanoparticles in microgels prepared by stop-flow lithography. J Am Chem Soc, 2012, 134(17): 7337-7343.
15.	An H Z, Helgeson M E, Doyle P S. Nanoemulsion composite microgels for orthogonal encapsulation and release. Adv Mater, 2012, 24(28): 3838-3844, 3895.
16.	Kwak M K, Jeong H E, Suh K Y. Rational design and enhanced biocompatibility of a dry adhesive medical skin patch. Adv Mater, 2011, 23(34): 3949-3953.
17.	Baik S, Kim J, Lee H J, et al. Highly adaptable and biocompatible octopus-like adhesive patches with meniscus-controlled unfoldable 3D microtips for underwater surface and hairy skin. Adv Sci, 2018, 5(8). DOI: 10.1002/advs.201800100.
18.	Chang Wanyi, Wu You, Chung Y C. Facile fabrication of ordered nanostructures from protruding nanoballs to recessional nanosuckers via solvent treatment on covered nanosphere assembled monolayers. Nano Lett, 2014, 14(3): 1546-1550.
19.	Campo A, Greiner C, Álvarez I, et al. Patterned surfaces with pillars with controlled 3D tip geometry mimicking bioattachment devices. Advanced Materials, 2007, 19(15): 1973-1977.
20.	Choi M K, Park O K, Choi C, et al. Cephalopod-inspired miniaturized suction cups for smart medical skin. Adv Healthc Mater, 2016, 5(1): 80-87.
21.	Lee B P, Messersmith P B, Israelachvili J N, et al. Mussel-inspired adhesives and coatings. Annu Rev Mater Res, 2011, 41(1): 99-132.
22.	Kord Forooshani P, Lee B P. Recent approaches in designing bioadhesive materials inspired by mussel adhesive protein. J Polym Sci A Polym Chem, 2017, 55(1): 9-33.
23.	Lee H, Scherer N F, Messersmith P B. Single-molecule mechanics of mussel adhesion. Proc Natl Acad Sci U S A, 2006, 103(35): 12999-13003.
24.	Yu Jing, Wei Wei, Menyo M S, et al. Adhesion of mussel foot protein-3 to TiO₂ surfaces: the effect of pH. Biomacromolecules, 2013, 14(4): 1072-1077.
25.	Lu Qingye, Danner E, Waite J H, et al. Adhesion of mussel foot proteins to different substrate surfaces. Journal of the Royal Society Interface, 2013, 10(79): 20120759.
26.	Li Shaochun, Chu Lina, Gong Xueqing, et al. Hydrogen bonding controls the dynamics of catechol adsorbed on a TiO₂(110) surface. Science, 2010, 328(5980): 882-884.
27.	Leng Chuan, Liu Yuwei, Jenkins C, et al. Interfacial structure of a DOPA-inspired adhesive polymer studied by sum frequency generation vibrational spectroscopy. Langmuir, 2013, 29(22): 6659-6664.
28.	McDowell L M, Burzio L A, Waite J H, et al. Rotational echo double resonance detection of cross-links formed in mussel byssus under high-flow stress. J Biol Chem, 1999, 274(29): 20293-20295.
29.	Hedlund J, Andersson M, Fant C, et al. Change of colloidal and surface properties of Mytilus edulis foot protein 1 in the presence of an oxidation (NaIO₄) or a complex-binding (Cu²⁺) agent. Biomacromolecules, 2009, 10(4): 845-849.
30.	Burzio L A, Waite J H. Cross-linking in adhesive quinoproteins: studies with model decapeptides. Biochemistry, 2000, 39(36): 11147-11153.
31.	Fan Changjiang, Fu Jiayin, Zhu Wenzhen, et al. A mussel-inspired double-crosslinked tissue adhesive intended for internal medical use. Acta Biomater, 2016, 33: 51-63.
32.	Ji Yali, Ji Ting, Liang Kai, et al. Mussel-inspired soft-tissue adhesive based on poly(diol citrate) with catechol functionality. J Mater Sci Mater Med, 2016, 27(2): 30.
33.	Rose S, Prevoteau A, Elzière P, et al. Nanoparticle solutions as adhesives for gels and biological tissues. Nature, 2014, 505(7483): 382-385.
34.	Pandey N, Hakamivala A, Xu Cancan, et al. Biodegradable nanoparticles enhanced adhesiveness of mussel-like hydrogels at tissue interface. Adv Healthc Mater, 2018, 7(7). DOI: 10.1002/adhm.201701069.
35.	Xu Yiwen, Liang Kai, Ullah W, et al. Chitin nanocrystal enhanced wet adhesion performance of mussel-inspired citrate-based soft-tissue adhesive. Carbohydr Polym, 2018, 190: 324-330.
36.	Kim H J, Yang B, Park T Y, et al. Complex coacervates based on recombinant mussel adhesive proteins: their characterization and applications. Soft Matter, 2017, 13(42): 7704-7716.
37.	Pangon A, Saesoo S, Saengkrit N A, et al. Hydroxyapatite-hybridized chitosan/chitin whisker bionanocomposite fibers for bone tissue engineering applications. Carbohydr Polym, 2016, 144: 419-427.
38.	Plat V D, Bootsma B T, Van Der Wielen N, et al. The role of tissue adhesives in esophageal surgery, a systematic review of literature. Int J Surg, 2017, 40: 163-168.
39.	Hafner D, Ziegler L, Ichwan M, et al. Mussel-inspired polymer carpets: direct photografting of polymer brushes on polydopamine nanosheets for controlled cell adhesion. Advanced Materials, 2016, 28(7): 1489-1494.
40.	Xu J, Strandman S, Zhu J X X, et al. Genipin-crosslinked catechol-chitosan mucoadhesive hydrogels for buccal drug delivery. Biomaterials, 2015, 37: 395-404.
41.	Park H J, Jin Y, Shin J, et al. Catechol-functionalized hyaluronic acid hydrogels enhance angiogenesis and osteogenesis of human adipose-derived stem cells in critical tissue defects. Biomacromolecules, 2016, 17(6): 1939-1948.
42.	牛睿. 光聚合仿生生物粘合剂的研究. 北京: 北京化工大学, 2011.
43.	Yang S Y, O'Cearbhaill E D, Sisk G C, et al. A bio-inspired swellable microneedle adhesive for mechanical interlocking with tissue. Nat Commun, 2013, 4(102(S1)): 1702.
44.	Li Ang, Jia Yunfei, Sun Shengtong, et al. Mineral-enhanced polyacrylic acid hydrogel as an oyster-inspired organic-inorganic hybrid adhesive. ACS Appl Mater Interfaces, 2018, 10(12): 10471-10479.
45.	Amjadi M, Turan M, Clementson C P, et al. Parallel microcracks based ultrasensitive and highly stretchable strain sensors. Acs Applied Materials & Interfaces, 2016, 8(8): 5618.
46.	Gao W, Emaminejad S, Nyein H Y, et al. Fully integrated wearable sensor arrays for multiplexed in situ perspiration analysis. Nature, 2016, 529(7587): 509-514.
47.	Mostafalu P, Akbari M, Alberti K A, et al. A toolkit of thread-based microfluidics, sensors, and electronics for 3D tissue embedding for medical diagnostics. Microsystems & Nanoengineering, 2016, 2: 16039.
48.	Drotlef D M, Amjadi M, Yunusa M, et al. Bioinspired Composite Microfibers for Skin Adhesion and Signal Amplification of Wearable Sensors[J]. Adv Mater, 2017, 29(28). DOI: 10.1002/adma.201701353.
49.	Wang H, Giorgia P, Chengkuo L. Toward self‐powered wearable adhesive skin patch with bendable microneedle array for transdermal drug delivery. Advanced Science, 2016, 3(9): 1500441.
50.	Hennebert E, Wattiez R, Demeuldre M, et al. Sea star tenacity mediated by a protein that fragments, then aggregates. Proceedings of the National Academy of Sciences of the United States of America, 2014, 111(17): 6317.
51.	Brennan M J, Kilbride B F, Wilker J J, et al. A bioinspired elastin-based protein for a cytocompatible underwater adhesive. Biomaterials, 2017, 124: 116-125.

1. Seo S, Lee D W, Ahn J S, et al. Significant performance enhancement of polymer resins by bioinspired dynamic bonding. Adv Mater, 2017, 29(39). DOI: 10.1002/adma.201703026.
2. Priemel T, Degtyar E, Dean M N, et al. Rapid self-assembly of complex biomolecular architectures during mussel byssus biofabrication. Nat Commun, 2017, 8: 14539.
3. Rapp M V, Maier G P, Dobbs H A, et al. Defining the catechol-cation synergy for enhanced wet adhesion to mineral surfaces. J Am Chem Soc, 2016, 138(29): 9013-9016.
4. Zhao Yanhua, Wu Yang, Wang Liang, et al. Bio-inspired reversible underwater adhesive. Nat Commun, 2017, 8(1): 2218.
5. Lee H, Um D S, Lee Y, et al. Octopus-inspired smart adhesive pads for transfer printing of semiconducting nanomembranes. Adv Mater, 2016, 28(34): 7457-7465.
6. Chen Yingchu, Yang Hongta. Octopus-inspired assembly of nanosucker arrays for dry/wet adhesion. ACS Nano, 2017, 11(6): 5332-5338.
7. Baik S, Kim D W, Park Y, et al. A wet-tolerant adhesive patch inspired by protuberances in suction cups of octopi. Nature, 2017, 546(7658): 396-400.
8. Chen L, An H Z, Haghgooie R, et al. Flexible octopus-shaped hydrogel particles for specific cell capture. Small, 2016, 12(15): 2001-2008.
9. Went P T, Lugli A, Meier S, et al. Frequent EpCam protein expression in human carcinomas. Hum Pathol, 2004, 35(1): 122-128.
10. Dendukuri D, Pregibon D C, Collins J, et al. Continuous-flow lithography for high-throughput microparticle synthesis. Nat Mater, 2006, 5(5): 365-369.
11. Dendukuri D, Gu S S, Pregibon D C, et al. Stop-flow lithography in a microfluidic device. Lab Chip, 2007, 7(7): 818-828.
12. Björnmalm M, Yan Y, Caruso F. Engineering and evaluating drug delivery particles in microfluidic devices. J Control Release, 2014, 190: 139-149.
13. Pregibon D C, Toner M, Doyle P S. Multifunctional encoded particles for high-throughput biomolecule analysis. Science, 2007, 315(5817): 1393-1396.
14. Suh S K, Yuet K, Hwang D K, et al. Synthesis of nonspherical superparamagnetic particles: in situ coprecipitation of magnetic nanoparticles in microgels prepared by stop-flow lithography. J Am Chem Soc, 2012, 134(17): 7337-7343.
15. An H Z, Helgeson M E, Doyle P S. Nanoemulsion composite microgels for orthogonal encapsulation and release. Adv Mater, 2012, 24(28): 3838-3844, 3895.
16. Kwak M K, Jeong H E, Suh K Y. Rational design and enhanced biocompatibility of a dry adhesive medical skin patch. Adv Mater, 2011, 23(34): 3949-3953.
17. Baik S, Kim J, Lee H J, et al. Highly adaptable and biocompatible octopus-like adhesive patches with meniscus-controlled unfoldable 3D microtips for underwater surface and hairy skin. Adv Sci, 2018, 5(8). DOI: 10.1002/advs.201800100.
18. Chang Wanyi, Wu You, Chung Y C. Facile fabrication of ordered nanostructures from protruding nanoballs to recessional nanosuckers via solvent treatment on covered nanosphere assembled monolayers. Nano Lett, 2014, 14(3): 1546-1550.
19. Campo A, Greiner C, Álvarez I, et al. Patterned surfaces with pillars with controlled 3D tip geometry mimicking bioattachment devices. Advanced Materials, 2007, 19(15): 1973-1977.
20. Choi M K, Park O K, Choi C, et al. Cephalopod-inspired miniaturized suction cups for smart medical skin. Adv Healthc Mater, 2016, 5(1): 80-87.
21. Lee B P, Messersmith P B, Israelachvili J N, et al. Mussel-inspired adhesives and coatings. Annu Rev Mater Res, 2011, 41(1): 99-132.
22. Kord Forooshani P, Lee B P. Recent approaches in designing bioadhesive materials inspired by mussel adhesive protein. J Polym Sci A Polym Chem, 2017, 55(1): 9-33.
23. Lee H, Scherer N F, Messersmith P B. Single-molecule mechanics of mussel adhesion. Proc Natl Acad Sci U S A, 2006, 103(35): 12999-13003.
24. Yu Jing, Wei Wei, Menyo M S, et al. Adhesion of mussel foot protein-3 to TiO₂ surfaces: the effect of pH. Biomacromolecules, 2013, 14(4): 1072-1077.
25. Lu Qingye, Danner E, Waite J H, et al. Adhesion of mussel foot proteins to different substrate surfaces. Journal of the Royal Society Interface, 2013, 10(79): 20120759.
26. Li Shaochun, Chu Lina, Gong Xueqing, et al. Hydrogen bonding controls the dynamics of catechol adsorbed on a TiO₂(110) surface. Science, 2010, 328(5980): 882-884.
27. Leng Chuan, Liu Yuwei, Jenkins C, et al. Interfacial structure of a DOPA-inspired adhesive polymer studied by sum frequency generation vibrational spectroscopy. Langmuir, 2013, 29(22): 6659-6664.
28. McDowell L M, Burzio L A, Waite J H, et al. Rotational echo double resonance detection of cross-links formed in mussel byssus under high-flow stress. J Biol Chem, 1999, 274(29): 20293-20295.
29. Hedlund J, Andersson M, Fant C, et al. Change of colloidal and surface properties of Mytilus edulis foot protein 1 in the presence of an oxidation (NaIO₄) or a complex-binding (Cu²⁺) agent. Biomacromolecules, 2009, 10(4): 845-849.
30. Burzio L A, Waite J H. Cross-linking in adhesive quinoproteins: studies with model decapeptides. Biochemistry, 2000, 39(36): 11147-11153.
31. Fan Changjiang, Fu Jiayin, Zhu Wenzhen, et al. A mussel-inspired double-crosslinked tissue adhesive intended for internal medical use. Acta Biomater, 2016, 33: 51-63.
32. Ji Yali, Ji Ting, Liang Kai, et al. Mussel-inspired soft-tissue adhesive based on poly(diol citrate) with catechol functionality. J Mater Sci Mater Med, 2016, 27(2): 30.
33. Rose S, Prevoteau A, Elzière P, et al. Nanoparticle solutions as adhesives for gels and biological tissues. Nature, 2014, 505(7483): 382-385.
34. Pandey N, Hakamivala A, Xu Cancan, et al. Biodegradable nanoparticles enhanced adhesiveness of mussel-like hydrogels at tissue interface. Adv Healthc Mater, 2018, 7(7). DOI: 10.1002/adhm.201701069.
35. Xu Yiwen, Liang Kai, Ullah W, et al. Chitin nanocrystal enhanced wet adhesion performance of mussel-inspired citrate-based soft-tissue adhesive. Carbohydr Polym, 2018, 190: 324-330.
36. Kim H J, Yang B, Park T Y, et al. Complex coacervates based on recombinant mussel adhesive proteins: their characterization and applications. Soft Matter, 2017, 13(42): 7704-7716.
37. Pangon A, Saesoo S, Saengkrit N A, et al. Hydroxyapatite-hybridized chitosan/chitin whisker bionanocomposite fibers for bone tissue engineering applications. Carbohydr Polym, 2016, 144: 419-427.
38. Plat V D, Bootsma B T, Van Der Wielen N, et al. The role of tissue adhesives in esophageal surgery, a systematic review of literature. Int J Surg, 2017, 40: 163-168.
39. Hafner D, Ziegler L, Ichwan M, et al. Mussel-inspired polymer carpets: direct photografting of polymer brushes on polydopamine nanosheets for controlled cell adhesion. Advanced Materials, 2016, 28(7): 1489-1494.
40. Xu J, Strandman S, Zhu J X X, et al. Genipin-crosslinked catechol-chitosan mucoadhesive hydrogels for buccal drug delivery. Biomaterials, 2015, 37: 395-404.
41. Park H J, Jin Y, Shin J, et al. Catechol-functionalized hyaluronic acid hydrogels enhance angiogenesis and osteogenesis of human adipose-derived stem cells in critical tissue defects. Biomacromolecules, 2016, 17(6): 1939-1948.
42. 牛睿. 光聚合仿生生物粘合剂的研究. 北京: 北京化工大学, 2011.
43. Yang S Y, O'Cearbhaill E D, Sisk G C, et al. A bio-inspired swellable microneedle adhesive for mechanical interlocking with tissue. Nat Commun, 2013, 4(102(S1)): 1702.
44. Li Ang, Jia Yunfei, Sun Shengtong, et al. Mineral-enhanced polyacrylic acid hydrogel as an oyster-inspired organic-inorganic hybrid adhesive. ACS Appl Mater Interfaces, 2018, 10(12): 10471-10479.
45. Amjadi M, Turan M, Clementson C P, et al. Parallel microcracks based ultrasensitive and highly stretchable strain sensors. Acs Applied Materials & Interfaces, 2016, 8(8): 5618.
46. Gao W, Emaminejad S, Nyein H Y, et al. Fully integrated wearable sensor arrays for multiplexed in situ perspiration analysis. Nature, 2016, 529(7587): 509-514.
47. Mostafalu P, Akbari M, Alberti K A, et al. A toolkit of thread-based microfluidics, sensors, and electronics for 3D tissue embedding for medical diagnostics. Microsystems & Nanoengineering, 2016, 2: 16039.
48. Drotlef D M, Amjadi M, Yunusa M, et al. Bioinspired Composite Microfibers for Skin Adhesion and Signal Amplification of Wearable Sensors[J]. Adv Mater, 2017, 29(28). DOI: 10.1002/adma.201701353.
49. Wang H, Giorgia P, Chengkuo L. Toward self‐powered wearable adhesive skin patch with bendable microneedle array for transdermal drug delivery. Advanced Science, 2016, 3(9): 1500441.
50. Hennebert E, Wattiez R, Demeuldre M, et al. Sea star tenacity mediated by a protein that fragments, then aggregates. Proceedings of the National Academy of Sciences of the United States of America, 2014, 111(17): 6317.
51. Brennan M J, Kilbride B F, Wilker J J, et al. A bioinspired elastin-based protein for a cytocompatible underwater adhesive. Biomaterials, 2017, 124: 116-125.

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