Bioinspired super-strong aqueous synthetic tissue adhesives
Open accessAbstract
Existing tissue adhesives and sealants are far from satisfactory when applied on wet and dynamic tissues. Herein, we report a strategy for designing biodegradable super-strong aqueous glue (B-Seal) for surgical uses inspired by an English ivy adhesion strategy and a cement particle packing theory. B-Seal is a fast-gelling, super-strong, and elastic adhesive sealant composed of injectable water-borne biodegradable polyurethane (WPU) nanodispersions with mismatched particle sizes and counterions in its A-B formulation. B-Seal showed 24-fold greater burst pressure than DuraSeal®, 138-fold greater T-pull adhesive strength than fibrin glue, and 16-fold greater lap shear strength than fibrin glue. In vivo evaluation on a rat cerebrospinal fluid (CSF) rhinorrhea model and a porcine craniotomy model validated the safety and efficacy of B-Seal for effective CSF leak prevention and dura repair. The plant-inspired adhesion strategy combined with particle packing theory represents a new direction of designing the next-generation wet tissue adhesives for surgeries.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Compared with clinical sutures, tissue adhesives show advantages in ease of use, sealing of air/fluid leakage, and less pain and scars.
“Compared with clinical sutures, tissue adhesives show advantages in ease of use, sealing of air/fluid leakage, and less pain and scars [97,98].”
From Mussel-Inspired Injectable Adhesive Hydrogels for Biomedical Applications (2024) · cites this paper as [98]
The Introduction (page unavailable) describes tissue adhesives as alternatives to sutures because of their ease of use, airtight or watertight sealing, and minimal tissue damage. It does not establish that adhesives cause less pain or fewer scars than sutures; the Results’ observation of no excessive scar tissue after B-Seal implantation is not a comparison with sutures. (LLM, conf=0.86)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Skin-inspired hydrogel–elastomer hybrids with robust interfaces and functional microstructures
Yuk, H., Zhang, T., Parada, G. A., Liu, X., & Zhao, X. (2016) · Nature Communications · doi:10.1038/ncomms12028 · Cited by 1,035 · see citing works
Self-citationHuman Cartilage Repair with a Photoreactive Adhesive-Hydrogel Composite
Sharma, B., Fermanian, S., Gibson, M., Unterman, S., Herzka, D. A., Cascio, B., Coburn, J., Hui, A. Y., Marcus, N., Gold, G. E., et al. (2013) · Science Translational Medicine · doi:10.1126/scitranslmed.3004838 · Cited by 342 · see citing works
Flagged first, then by citations
Research works printed but not linked: 50
- [2]Li J, Celiz AD, Yang J, Yang Q, Wamala I, Whyte W, Seo BR, Vasilyev NV, Vlassak JJ, Suo Z, and Mooney DJ (2017). Tough adhesives for diverse wet surfaces. Science 357, 378– 381. 28751604 PMC5905340
- [3]Singer AJ, and Thode HC Jr. (2004). A review of the literature on octylcyanoacrylate tissue adhesive. Am J Surg 187, 238– 248. 14769312
- [4]Ma C, Sun J, Li B, Feng Y, Sun Y, Xiang L, Wu B, Xiao L, Liu B, Petrovskii VS, Bin L, Zhang J, Wang Z, Li H, Zhang L, Li J, Wang F, Gstl R, Potemkin II, Chen D, Zeng H, Zhang H, Liu K, and Herrmann A. (2021). Ultra-strong bio-glue from genetically engineered polypeptides. Nat Commun 12, 3613. 34127656 PMC8203747
- [5]Sani ES, Kheirkhah A, Rana D, Sun ZM, Foulsham W, Sheikhi A, Khademhosseini A, Dana R, and Annabi N. (2019). Sutureless repair of corneal injuries using naturally derived bioadhesive hydrogels. Sci Adv 5. PMC6426459 30906864
- [6]Guo YC, Wang Y, Zhao XH, Li X, Wang Q, Zhong W, Mequanint K, Zhan RX, Xing M, and Luo GX (2021). Snake extract-laden hemostatic bioadhesive gel cross- linked by visible light. Sci Adv 7. PMC8279511 34261653
- [7]Sani ES, Lara RP, Aldawood Z, Bassir SH, Nguyen D, Kantarci A, Intini G, and Annabi N. (2019). An Antimicrobial Dental Light Curable Bioadhesive Hydrogel for Treatment of Peri-Implant Diseases. Matter 1, 926– 944. 31663080 PMC6818244
- [10]Bhagat V, and Becker ML (2017). Degradable Adhesives for Surgery and Tissue Engineering. Biomacromolecules 18, 3009– 3039. 28862846
- [11]Zhao YH, Wu Y, Wang L, Zhang MM, Chen X, Liu MJ, Fan J, Liu JQ, Zhou F, and Wang ZK (2017). Bio-inspired reversible underwater adhesive. Nature Communications 8. PMC5738439 29263405
- [15]von Byern J, Grunwald I, Kosok M, Saporito RA, Dicke U, Wetjen O, Thiel K, Borcherding K, Kowalik T, and Marchetti-Deschmann M. (2017). Chemical characterization of the adhesive secretions of the salamander Plethodon shermani (Caudata, Plethodontidae). Sci Rep-Uk 7. PMC5532285 28751633
- [16]Lee BP, Dalsin JL, and Messersmith PB (2002). Synthesis and gelation of DOPA- modified poly(ethylene glycol) hydrogels. Biomacromolecules 3, 1038– 1047. 12217051
- [18]Ma YF, Ma SH, Wu Y, Pei XW, Gorb SN, Wang ZK, Liu WM, and Zhou F. (2018). Remote Control over Underwater Dynamic Attachment/Detachment and Locomotion. Adv Mater 30. 29921014
- [19]Maier GP, Rapp MV, Waite JH, Israelachvili JN, and Butler A. (2015). Adaptive synergy between catechol and lysine promotes wet adhesion by surface salt displacement. Science 349, 628– 632. 26250681
- [20]Yuk H, Varela CE, Nabzdyk CS, Mao XY, Padera RF, Roche ET, and Zhao XH (2019). Dry double-sided tape for adhesion of wet tissues and devices. Nature 575, 169-+. 31666696
- [21]Guo J, Kim GB, Shan D, Kim JP, Hu J, Wang W, Hamad FG, Qian G, Rizk EB, and Yang J. (2017). Click chemistry improved wet adhesion strength of mussel- inspired citrate-based antimicrobial bioadhesives. Biomaterials 112, 275– 286. 27770631 PMC5121090
- [22]Guo J, Wang W, Hu J, Xie D, Gerhard E, Nisic M, Shan D, Qian G, Zheng S, and Yang J. (2016). Synthesis and characterization of anti-bacterial and anti-fungal citrate-based mussel-inspired bioadhesives. Biomaterials 85, 204– 217. 26874283 PMC4764444
- [23]Lu X, Shi S, Li H, Gerhard E, Lu Z, Tan X, Li W, Rahn KM, Xie D, Xu G, Zou F, Bai X, Guo J, and Yang J. (2020). Magnesium oxide-crosslinked low-swelling citrate-based mussel-inspired tissue adhesives. Biomaterials 232, 119719. 31901688
- [24]Guo J, Sun W, Kim JP, Lu X, Li Q, Lin M, Mrowczynski O, Rizk EB, Cheng J, Qian G, and Yang J. (2018). Development of tannin-inspired antimicrobial bioadhesives. Acta Biomater 72, 35– 44. 29555464 PMC6328059
- [25]Huang Y, Wang Y, Tan L, Sun L, Petrosino J, Cui M-Z, Hao F, and Zhang M. (2016). Nanospherical arabinogalactan proteins are a key component of the high-strength adhesive secreted by English ivy. Proceedings of the National Academy of Sciences 113, E3193– E3202. PMC4988582 27217558
- [26]Wong V, Chan KW, and Kwan AKH (2013). Applying Theories of Particle Packing and Rheology to Concrete for Sustainable Development. organization, technology and management in construction · an international journal 5, 844– 851.
- [30]Daniel-da-Silva AL, Moura Bordado JC, and Martin-Martinez JM (2008). Moisture curing kinetics of isocyanate ended urethane quasi-prepolymers monitored by IR Spectroscopy and DSC. Journal of Applied Polymer Science 107, 700– 709.
- [32]Garcia R. (2020). Nanomechanical mapping of soft materials with the atomic force microscope: methods, theory and applications. Chem Soc Rev 49, 5850– 5884. 32662499
- [33]Dokukin ME, and Sokolov I. (2012). Quantitative mapping of the elastic modulus of soft materials with HarmoniX and PeakForce QNM AFM modes. Langmuir 28, 16060– 16071. 23113608
- [34]Nishihira S, and McCaffrey TV (1988). The use of fibrin glue for the repair of experimental csf rhinorrhea. The Laryngoscope 98, 625– 627. 2453770
- [35]Oh JW, Kim SH, and Whang K. (2017). Traumatic Cerebrospinal Fluid Leak: Diagnosis and Management. Korean J Neurotrauma 13, 63– 67. 29201836 PMC5702760
- [36]Esposito F, Angileri FF, Kruse P, Cavallo LM, Solari D, Esposito V, Tomasello F, and Cappabianca P. (2016). Fibrin Sealants in Dura Sealing: A Systematic Literature Review. PLOS ONE 11, e0151533. PMC4847933 27119993
- [37]Kawai H, Nakagawa I, Nishimura F, Motoyama Y, Park Y-S, Nakamura M, Nakase H, Suzuki S, and Ikada Y. (2014). Usefulness of a New Gelatin Glue Sealant System for Dural Closure in a Rat Durotomy Model. Neurologia medico-chirurgica 54, 640– 646. 25070015 PMC4533497
- [38]Reece TB, Maxey TS, and Kron IL (2001). A prospectus on tissue adhesives. American Journal of Surgery 182, 40S– 44S. 11566476
- [39]Epstein NE (2010). Dural repair with four spinal sealants: focused review of the manufacturers inserts and the current literature. The Spine Journal 10, 1065– 1068. 21094467
- [40]Zoia C, Bongetta D, Lombardi F, Custodi VM, Pugliese R, and Gaetani P. (2015). First impressions about Adherus, a new dural sealant. Journal of Applied Biomaterials & Functional Materials 13, e372– 375. 26350346
- [41]Annabi N, Yue K, Tamayol A, and Khademhosseini A. (2015). Elastic sealants for surgical applications. European Journal of Pharmaceutics and Biopharmaceutics 95, 27– 39. 26079524 PMC4591192
- [42]Mehdizadeh M, Weng H, Gyawali D, Tang L, and Yang J. (2012). Injectable citrate- based mussel-inspired tissue bioadhesives with high wet strength for sutureless wound closure. Biomaterials 33, 7972– 7983. 22902057 PMC3432175
- [43]Mehdizadeh M, and Yang J. (2013). Design Strategies and Applications of Tissue Bioadhesives. Macromolecular Bioscience 13, 271– 288. 23225776 PMC3660144
- [44]Lee G, Lee CK, and Bynevelt M. (2010). DuraSeal-hematoma: concealed hematoma causing spinal cord compression. Spine (Phila Pa 1976) 35, E1522– 1524. 21102284
- [45]Bernal-Sprekelsen M, Alobid I, Mullol J, Trobat F, and Tomas-Barberan M. (2005). Closure of cerebrospinal fluid leaks prevents ascending bacterial meningitis. Rhinology 43, 277– 281. 16405272
- [46]Preul MC, Campbell PK, Bichard WD, and Spetzler RF (2007). Application of a hydrogel sealant improves watertight closures of duraplasty onlay grafts in a canine craniotomy model. J Neurosurg 107, 642– 650. 17886566
- [47]Rose S, Prevoteau A, Elziere P, Hourdet D, Marcellan A, and Leibler L. (2014). Nanoparticle solutions as adhesives for gels and biological tissues. Nature 505, 382-+. 24336207
- [48]Tang JD, Li JY, Vlassak JJ, and Suo ZG (2016). Adhesion between highly stretchable materials. Soft Matter 12, 1093– 1099. 26573427
- [49]Kurokawa T, Furukawa H, Wang W, Tanaka Y, and Gong JP (2010). Formation of a strong hydrogel-porous solid interface via the double-network principle. Acta Biomaterialia 6, 1353– 1359. 19887124
- [50]Cha CY, Antoniadou E, Lee M, Jeong JH, Ahmed WW, Saif TA, Boppart SA, and Kong H. (2013). Tailoring Hydrogel Adhesion to Polydimethylsiloxane Substrates Using Polysaccharide Glue. Angewandte Chemie-International Edition 52, 6949– 6952. 23729395
- [51]Roy CK, Guo HL, Sun TL, Bin Ihsan A, Kurokawa T, Takahata M, Nonoyama T, Nakajima T, and Gong JP (2015). Self-Adjustable Adhesion of Polyampholyte Hydrogels. Adv Mater 27, 7344-+. 26459267
- [53]Pawlicki JM, Pease LB, Pierce CM, Startz TP, Zhang Y, and Smith AM (2004). The effect of molluscan glue proteins on gel mechanics. J Exp Biol 207, 1127– 1135. 14978055
- [54]Wilks AM, Rabice SR, Garbacz HS, Harro CC, and Smith AM (2015). Double-network gels and the toughness of terrestrial slug glue. J Exp Biol 218, 3128– 3137. 26276864
- [55]Rickett TA, Amoozgar Z, Tuchek CA, Park J, Yeo Y, and Shi R. (2011). Rapidly photo-cross-linkable chitosan hydrogel for peripheral neurosurgeries. Biomacromolecules 12, 57– 65. 21128673
- [56]Horio T, Ishihara M, Fujita M, Kishimoto S, Kanatani Y, Ishizuka T, Nogami Y, Nakamura S, Tanaka Y, Morimoto Y, and Maehara T. (2010). Effect of photocrosslinkable chitosan hydrogel and its sponges to stop bleeding in a rat liver injury model. Artif Organs 34, 342– 347. 20420617
- [57]Mogal V, Papper V, Chaurasia A, Feng G, Marks R, and Steele T. (2014). Novel on-demand bioadhesion to soft tissue in wet environments. Macromol Biosci 14, 478– 484. 24293270
- [58]Elvin CM, Vuocolo T, Brownlee AG, Sando L, Huson MG, Liyou NE, Stockwell PR, Lyons RE, Kim M, Edwards GA, Johnson G, McFarland GA, Ramshaw JAM, and Werkmeister JA (2010). A highly elastic tissue sealant based on photopolymerised gelatin. Biomaterials 31, 8323– 8331. 20674967
- [59]International Commission on Non-Ionizing Radiation, P. (2004). Guidelines on limits of exposure to ultraviolet radiation of wavelengths between 180 nm and 400 nm (incoherent optical radiation). Health Phys 87, 171– 186. 15257218
- [60]Melzer B, Steinbrecher T, Seidel R, Kraft O, Schwaiger R, and Speck T. (2010). The attachment strategy of English ivy: a complex mechanism acting on several hierarchical levels. Journal of the Royal Society Interface 7, 1383– 1389. PMC2894893 20462880
- [62]Maiti R, Duan MQ, Danby SG, Lewis R, Matcher SJ, and Carre MJ (2020). Morphological parametric mapping of 21 skin sites throughout the body using optical coherence tomography. J Mech Behav Biomed 102. 31877514
- [64]Hafeman AE, Zienkiewicz KJ, Zachman AL, Sung HJ, Nanney LB, Davidson JM, and Guelcher SA (2011). Characterization of the degradation mechanisms of lysine-derived aliphatic poly(ester urethane) scaffolds. Biomaterials 32, 419– 429. 20864156 PMC2997347
Cited by
Sorted by citations
Mussel-Inspired Injectable Adhesive Hydrogels for Biomedical Applications
Dou, W., Zeng, X., Zhu, S., Zhu, Y., Liu, H., & Li, S. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25169100 · Cited by 52 · see citing works
- Authors
- Li, Q., Song, W., Li, J., Ma, C., Zhao, X., Jiao, J., Mrowczynski, O., Webb, B. S., Rizk, E. B., Lu, D., & Liu, C.
- Affiliations
- Kunming Medical University (CN)
- Pennsylvania State University (US)
- Corresponding author
- Rizk, Elias B.
- Liu, Chao
- ORCID
- Venue
- Matter
- Publisher
- Elsevier BV
- Published
- 2022-03
- Volume
- 5
- Issue
- 3
- Pages
- 933-956
- ISSN
- 2590-2385 (ISSN-L)
- PMC
- PMC8896806
- OpenAlex
- W4207030627
- Cited by
- 58
- References
- 2
- Citations by year
- 2026: 16 · 2025: 17 · 2024: 15 · 2023: 7 · 2022: 3
- FWCI
- 10.04
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 366 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Matter (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- National Institute of General Medical Sciences
- Small Business Innovation Research (R43 GM130231)
- Topics
- Health Sciences › Medicine › Surgery › Surgical Sutures and Adhesives
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Medicine › Hydrogels: synthesis, properties, applications
- Physical Sciences › Materials Science › Biomaterials › biodegradable polymer synthesis and properties
- Keywords
- tissue adhesives, aqueous adhesives, biodegradable polyurethane, nanoparticle dispersion, counterions, burst pressure, lap shear strength, fibrin glue, cerebrospinal fluid leak, surgical sealants, wet tissue adhesion
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review