Abstract
Purpose
Based on the clinical need for grafts for vascular tissue regeneration, our group developed a customizable scaffold derived from the human amniotic membrane. Our approach consists of rolling the decellularized amniotic membrane around a mandrel to form a multilayered tubular scaffold with tunable diameter and wall thickness. Herein, we aimed to investigate if silica nanoparticles (SiNP) could enhance the adhesion of the amnion layers within these rolled grafts.
Methods
To test this, we assessed the structural integrity and mechanical properties of SiNP-treated scaffolds. Mechanical tests were repeated after six months to evaluate adhesion stability in aqueous environments.
Results
Our results showed that the rolled SiNP-treated scaffolds maintained their tubular shape upon hydration, while non-treated scaffolds collapsed. By scanning electron microscopy, SiNP-treated scaffolds presented more densely packed layers than untreated controls. Mechanical analysis showed that SiNP treatment increased the scaffold’s tensile strength up to tenfold in relation to non-treated controls and changed the mechanism of failure from interfacial slipping to single-point fracture. The nanoparticles reinforced the scaffolds both at the interface between two distinct layers and within each layer of the extracellular matrix. Finally, SiNP-treated scaffolds significantly increased the suture pullout force in comparison to untreated controls.
Conclusion
Our study demonstrated that SiNP prevents the unraveling of a multilayered extracellular matrix graft while improving the scaffolds’ overall mechanical properties. In addition to the generation of a robust biomaterial for vascular tissue regeneration, this novel layering technology is a promising strategy for a number of bioengineering applications.
Similar content being viewed by others
Data availability
The data that support the findings of this study are available from the corresponding author upon reasonable request.
References
AAMI (2001) ANSI/AAMI/ISO 7198:1998/2001/(R)2004 Cardiovascular implants—Tubular vascular prostheses
Abousleiman RI, Reyes Y, McFetridge P, Sikavitsas V (2008) The human umbilical vein: a novel scaffold for musculoskeletal soft tissue regeneration. Artif Organs 32:735–741. https://doi.org/10.1111/j.1525-1594.2008.00598.x
Amensag S, McFetridge PS (2012) Rolling the human amnion to engineer laminated vascular tissues. Tissue Eng Part C Methods 18:903–912. https://doi.org/10.1089/ten.tec.2012.0119
Amensag S, McFetridge PS (2014) Tuning scaffold mechanics by laminating native extracellular matrix membranes and effects on early cellular remodeling. J Biomed Mater Res Part A 102:1325–1333. https://doi.org/10.1002/jbm.a.34791
Amensag S, Goldberg LA, O’Malley KA et al (2017) Pilot assessment of a human extracellular matrix-based vascular graft in a rabbit model. J Vasc Surg 65:839. https://doi.org/10.1016/j.jvs.2016.02.046
Badylak SF, Freytes DO, Gilbert TW (2009) Extracellular matrix as a biological scaffold material: structure and function. Acta Biomater 5:1–13. https://doi.org/10.1016/j.actbio.2008.09.013
Camasão DB, Mantovani D (2021) The mechanical characterization of blood vessels and their substitutes in the continuous quest for physiological-relevant performances. A critical review. Mater Today Bio. https://doi.org/10.1016/j.mtbio.2021.100106
Cheng ZJ, So RP, Byung HC et al (2007) Human amniotic membrane as a delivery matrix for articular cartilage repair. Tissue Eng 13:693–702. https://doi.org/10.1089/ten.2006.0184
Cheung DT, Nimni ME (1982) Mechanism of crosslinking of proteins by glutaraldehyde II. Reaction with monomeric and polymeric collagen. Connect Tissue Res 10:201–216. https://doi.org/10.3109/03008208209034419
Crouzier T, McClendon T, Tosun Z, McFetridge PS (2009) Inverted human umbilical arteries with tunable wall thicknesses for nerve regeneration. J Biomed Mater Res Part A 89:818–828. https://doi.org/10.1002/jbm.a.32103
Daniel J, Abe K, McFetridge PS (2005) Development of the human umbilical vein scaffold for cardiovascular tissue engineering applications. ASAIO J 51:252–261. https://doi.org/10.1097/01.MAT.0000160872.41871.7E
Dardik H, Wengerter K, Qin F et al (2002) Comparative decades of experience with glutaraldehyde-tanned human umbilical cord vein graft for lower limb revascularization: an analysis of 1275 cases. J Vasc Surg 35:64–71. https://doi.org/10.1067/mva.2002.121053
Desimone MF, Hélary C, Rietveld IB et al (2010) Silica-collagen bionanocomposites as three-dimensional scaffolds for fibroblast immobilization. Acta Biomater 6:3998–4004. https://doi.org/10.1016/J.ACTBIO.2010.05.014
Eglin D, Coradin T, Giraud Guille MM et al (2005a) Collagen–silica hybrid materials: sodium silicate and sodium chloride effects on type I collagen fibrillogenesis. Biomed Mater Eng 15:43–50
Eglin D, Mosser G, Giraud-Guille MM et al (2005b) Type I collagen, a versatile liquid crystal biological template for silica structuration from nano- to microscopic scales. Soft Matter 1:129–131. https://doi.org/10.1039/B503019F
Elkhenany H, El-Derby A, Abd Elkodous M et al (2022) Applications of the amniotic membrane in tissue engineering and regeneration: the hundred-year challenge. Stem Cell Res Ther. https://doi.org/10.1186/s13287-021-02684-0
Gonçalves MC (2018) Sol-gel silica nanoparticles in medicine: a natural choice. Design, synthesis and products. Molecules. https://doi.org/10.3390/molecules23082021
Janjua TI, Cao Y, Yu C, Popat A (2021) Clinical translation of silica nanoparticles. Nat Rev Mater 6:1072–1074. https://doi.org/10.1038/s41578-021-00385-x
Karimi A, Navidbakhsh M, Shojaei A, Faghihi S (2013) Measurement of the uniaxial mechanical properties of healthy and atherosclerotic human coronary arteries. Mater Sci Eng C 33:2550–2554. https://doi.org/10.1016/j.msec.2013.02.016
Kim KM, Kim HM, Lee WJ et al (2014) Surface treatment of silica nanoparticles for stable and charge-controlled colloidal silica. Int J Nanomed 9:29–40. https://doi.org/10.2147/IJN.S57922
Konig G, McAllister TN, Dusserre N et al (2009) Mechanical properties of completely autologous human tissue engineered blood vessels compared to human saphenous vein and mammary artery. Biomaterials 30:1542–1550. https://doi.org/10.1016/j.biomaterials.2008.11.011
Kumar A, Chandra R, Reddy A et al (2015) Evaluation of clinical, antiinflammatory and antiinfective properties of amniotic membrane used for guided tissue regeneration: a randomized controlled trial. Dent Res J (isfahan) 12:127–135
Leal BBJ, Wakabayashi N, Oyama K et al (2021) Vascular tissue engineering: polymers and methodologies for small caliber vascular grafts. Front Cardiovasc Med 7:592361. https://doi.org/10.3389/fcvm.2020.592361
Maharajan VS, Shanmuganathan V, Currie A et al (2007) Amniotic membrane transplantation for ocular surface reconstruction: indications and outcomes. Clin Exp Ophthalmol 35:140–147. https://doi.org/10.1111/j.1442-9071.2006.01408.x
Mallis P, Papapanagiotou A, Katsimpoulas M et al (2020) Efficient differentiation of vascular smooth muscle cells from Wharton’s Jelly mesenchymal stromal cells using human platelet lysate: a potential cell source for small blood vessel engineering. World J Stem Cells 12:203–221. https://doi.org/10.4252/wjsc.v12.i3.203
Marcus AJ, Woodbury D (2008) Fetal stem cells from extra-embryonic tissues: do not discard: stem cells review series. J Cell Mol Med 12:730–742. https://doi.org/10.1111/j.1582-4934.2008.00221.x
Martínez-González B, Reyes-Hernández CG, Quiroga-Garza A et al (2017) Conduits used in coronary artery bypass grafting: a review of morphological studies. Ann Thorac Cardiovasc Surg 23:55–65. https://doi.org/10.5761/atcs.ra.16-00178
Mc Namara K, Alzubaidi H, Jackson JK (2019) Cardiovascular disease as a leading cause of death: how are pharmacists getting involved? Integr Pharm Res Pract 8:1–11. https://doi.org/10.2147/iprp.s133088
Meddahi-Pellé A, Legrand A, Marcellan A et al (2014) Organ repair, hemostasis, and in vivo bonding of medical devices by aqueous solutions of nanoparticles. Angew Chemie Int Ed 53:6369–6373. https://doi.org/10.1002/anie.201401043
Mligiliche N, Endo K, Okamoto K et al (2002) Extracellular matrix of human amnion manufactured into tubes as conduits for peripheral nerve regeneration. J Biomed Mater Res 63:591–600. https://doi.org/10.1002/jbm.10349
Murphy SV, Skardal A, Nelson RA et al (2020) Amnion membrane hydrogel and amnion membrane powder accelerate wound healing in a full thickness porcine skin wound model. Stem Cells Transl Med 9:80–92. https://doi.org/10.1002/sctm.19-0101
Nerem R (1999) Tissue engineering of vascular prosthetic grafts. Nat Med 5:1118–1118. https://doi.org/10.1038/13434
Orts-Gil G, Natte K, Drescher D et al (2011) Characterisation of silica nanoparticles prior to in vitro studies: from primary particles to agglomerates. J Nanoparticle Res 13:1593–1604. https://doi.org/10.1007/S11051-010-9910-9/FIGURES/9
Otsuka F, Yahagi K, Sakakura K, Virmani R (2013) Why is the mammary artery so special and what protects it from atherosclerosis? Ann Cardiothorac Surg 2:519–51926. https://doi.org/10.3978/j.issn.2225-319X.2013.07.06
Pashneh-Tala S, MacNeil S, Claeyssens F (2016) The tissue-engineered vascular graft—past, present, and future. Tissue Eng Part B Rev 22:68–100. https://doi.org/10.1089/ten.teb.2015.0100
Patra JK, Das G, Fraceto LF et al (2018) Nano based drug delivery systems: recent developments and future prospects 10 technology 1007 nanotechnology 03 chemical sciences 0306 physical chemistry (incl. structural) 03 chemical sciences 0303 macromolecular and materials chemistry 11 medical and He. J Nanobiotechnol 16:1–33
Pessolato AGT, Martins DDS, Ambrósio CE et al (2011) Propolis and amnion reepithelialise second-degree burns in rats. Burns 37:1192–1201. https://doi.org/10.1016/j.burns.2011.05.016
Rodriguez M, Juran C, McClendon M et al (2012) Development of a mechanically tuneable 3D scaffold for vascular reconstruction. J Biomed Mater Res Part A 100A:3480–3489. https://doi.org/10.1002/jbm.a.34267
Rose S, Prevoteau A, Elzière P et al (2014) Nanoparticle solutions as adhesives for gels and biological tissues. Nature 505:382. https://doi.org/10.1038/nature12806
Saikia J, Mohammadpour R, Yazdimamaghani M et al (2018) Silica nanoparticle-endothelial interaction: uptake and effect on platelet adhesion under flow conditions. ACS Appl Bio Mater 1:1620–1627. https://doi.org/10.1021/acsabm.8b00466
Shammas NW, Radaideh Q, John Shammas W et al (2019) The role of precise imaging with intravascular ultrasound in coronary and peripheral interventions. Vasc Health Risk Manag 15:283–290. https://doi.org/10.2147/VHRM.S210928
Stekelenburg M, Rutten MCM, Snoeckx LHEH, Baaijens FPT (2009) Dynamic straining combined with fibrin gel cell seeding improves strength of tissue-engineered small-diameter vascular grafts. Tissue Eng Part A 15:1081–1089. https://doi.org/10.1089/ten.tea.2008.0183
Wilshaw SP, Kearney JN, Fisher J, Ingham E (2006) Production of an acellular amniotic membrane matrix for use in tissue engineering. Tissue Eng 12:2117–2129. https://doi.org/10.1089/ten.2006.12.2117
Wong V, Gada S, Singh M, Merna N (2023) The development of small-caliber vascular grafts using human umbilical artery: an evaluation of methods. Tissue Eng Part C Methods 29:1–10. https://doi.org/10.1089/ten.tec.2022.0144
Zhang H, Dunphy DR, Jiang X et al (2012) Processing pathway dependence of amorphous silica nanoparticle toxicity: colloidal vs pyrolytic. J Am Chem Soc 134:15790–15804. https://doi.org/10.1021/ja304907c
Acknowledgements
Special thanks to Kimberly Backer-Kelley of the Interdisciplinary Center for Biotechnology Research for her support at the Electron Microscopy core lab. UF Health Shands Labor & Delivery unit. Dr. Dara Wakefield and Louis Kauo of the UF Health Shands Department of Pathology.
Funding
Financial support provided by the National Institute of Health (NIH R01 HL088207).
Author information
Authors and Affiliations
Contributions
LAG: Performed experiments, analyzed the data and wrote the paper; HDZ: analyzed the data and wrote the paper; CM: performed experiments; PM: supervised the study, analyzed the data and wrote the paper.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no relevant financial or non-financial interests to disclose.
Ethical approval
Placental tissues were obtained from the Labor & Delivery department at UF Health Shands Hospital at the University of Florida (Gainesville, FL, IRB approval #64-2010).
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
10529_2024_3469_MOESM1_ESM.tif
Supplementary file1 (TIF 1048 KB)—Characterization of Ludox TM-50 Nanoparticles. a) Transmission electron microscopic image showed particle diameters of approximately 25 nm. b) Absorbance spectra of Ludox® TM-50 nanoparticle dispersions prepared in H2O. Magnification: 200,000x. Scale bar represents 100 nm
10529_2024_3469_MOESM2_ESM.tif
Supplementary file2 (TIF 236 KB)—Silica retention. The maximum retention and stability of nanoparticle-ECM interaction were studied both with and without lyophilization. Single-layered sections of freeze-dried amniotic ECM were incubated for 60 s in 0.7 mg/ml Ludox TM50 SiNP under gentle agitation. Half of the samples were subsequently incubated in water on an orbital shaker plate for 30 min. The other samples were lyophilized for 48 h prior to the 30 min incubation in water. Silica retention was determined based on the change in weight following the wash in water using the following equation:\(Silica\,retained \left( {\frac{\mu g}{{mm^{2} }}} \right) = \frac{{\left( {W{-}W_{0} } \right)}}{scaffold\,dimensions},\) where W represents the dry weight of the scaffold following the wash and lyophilization and W0 is the initial dry weight of the sample. The lyophilization step showed to be necessary for the retention of silica in the scaffolds, and the maximum retention was found to be 26.7 ± 5.55 μg/mm2
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Goldberg, L.A., Zomer, H.D., McFetridge, C. et al. Silica nanoparticles enhance interfacial self-adherence of a multi-layered extracellular matrix scaffold for vascular tissue regeneration. Biotechnol Lett 46, 469–481 (2024). https://doi.org/10.1007/s10529-024-03469-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10529-024-03469-0