Emerging Strategies for the Biofabrication of Multilayer Composite Amniotic Membranes for Biomedical Applications
Abstract
:1. Introduction
2. Amniotic Membrane Properties
2.1. Biological Properties
2.2. Physical and Mechanical Properties
3. Amniotic Membrane Collection, Processing, Preservation and Sterilization
4. Regenerative Properties of Amniotic Membrane to Treat Nerve Injuries
5. Multilayer Composite Amniotic Membranes and Applications
5.1. Additive Manufacturing Methods and Electrospinning
5.2. Electrospun Multilayered Composite Amniotic Membrane and Secondary Materials
5.3. Characterization of Electrospun Multilayered Composite-Based Amniotic Membrane
5.3.1. Mechanical Characterization
5.3.2. In Vitro and In Vivo Assessment of Electrospun Multilayered Composite-Based Amniotic Membrane
5.3.3. Application of Electrospun Multilayered Composite-Based Amniotic Membrane for Nerve Regeneration
6. Future Perspectives
7. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Bourne, G. The Foetal Membranes. A Review of the Anatomy of Normal Amnion and Chorion and Some Aspects of Their Function. Postgrad. Med. J. 1962, 38, 193–201. [Google Scholar] [CrossRef]
- Munoz-Torres, J.R.; Martínez-González, S.B.; Lozano-Luján, A.D.; Martínez-Vázquez, M.C.; Velasco-Elizondo, P.; Garza-Veloz, I.; Martinez-Fierro, M.L. Biological Properties and Surgical Applications of the Human Amniotic Membrane. Front. Bioeng. Biotechnol. 2022, 10, 1067480. [Google Scholar] [CrossRef]
- Fénelon, M.; Catros, S.; Meyer, C.; Fricain, J.-C.; Obert, L.; Auber, F.; Louvrier, A.; Gindraux, F. Applications of Human Amniotic Membrane for Tissue Engineering. Membranes 2021, 11, 387. [Google Scholar] [CrossRef] [PubMed]
- Davis, J.S., II. Skin Grafting at the Johns Hopkins Hospital. Ann. Surg. 1909, 50, 542–549. [Google Scholar] [CrossRef] [PubMed]
- Elkhenany, H.; El-Derby, A.; Abd Elkodous, M.; Salah, R.A.; Lotfy, A.; El-Badri, N. Applications of the Amniotic Membrane in Tissue Engineering and Regeneration: The Hundred-Year Challenge. Stem Cell Res. Ther. 2022, 13, 8. [Google Scholar] [CrossRef] [PubMed]
- Silini, A.R.; Cargnoni, A.; Magatti, M.; Pianta, S.; Parolini, O. The Long Path of Human Placenta, and Its Derivatives, in Regenerative Medicine. Front. Bioeng. Biotechnol. 2015, 3, 162. [Google Scholar] [CrossRef] [PubMed]
- Chen, L.; Song, X.; Yao, Z.; Zhou, C.; Yang, J.; Yang, Q.; Chen, J.; Wu, J.; Sun, Z.; Gu, L.; et al. Gelatin Nanofiber-Reinforced Decellularized Amniotic Membrane Promotes Axon Regeneration and Functional Recovery in the Surgical Treatment of Peripheral Nerve Injury. Biomaterials 2023, 300, 122207. [Google Scholar] [CrossRef] [PubMed]
- Leal-Marin, S.; Kern, T.; Hofmann, N.; Pogozhykh, O.; Framme, C.; Börgel, M.; Figueiredo, C.; Glasmacher, B.; Gryshkov, O. Human Amniotic Membrane: A Review on Tissue Engineering, Application, and Storage. J. Biomed. Mater. Res. B Appl. Biomater. 2021, 109, 1198–1215. [Google Scholar] [CrossRef] [PubMed]
- Dadkhah Tehrani, F.; Firouzeh, A.; Shabani, I.; Shabani, A. A Review on Modifications of Amniotic Membrane for Biomedical Applications. Front. Bioeng. Biotechnol. 2020, 8, 606982. [Google Scholar] [CrossRef]
- Sarvari, R.; Keyhanvar, P.; Agbolaghi, S.; Roshangar, L.; Bahremani, E.; Keyhanvar, N.; Haghdoost, M.; Keshel, S.H.; Taghikhani, A.; Firouzi, N.; et al. A Comprehensive Review on Methods for Promotion of Mechanical Features and Biodegradation Rate in Amniotic Membrane Scaffolds. J. Mater. Sci. Mater. Med. 2022, 33, 32. [Google Scholar] [CrossRef]
- Jahanafrooz, Z.; Bakhshandeh, B.; Behnam Abdollahi, S.; Seyedjafari, E. Human Amniotic Membrane as a Multifunctional Biomaterial: Recent Advances and Applications. J. Biomater. Appl. 2023, 37, 1341–1354. [Google Scholar] [CrossRef] [PubMed]
- Arrizabalaga, J.H.; Nollert, M.U. Human Amniotic Membrane: A Versatile Scaffold for Tissue Engineering. ACS Biomater. Sci. Eng. 2018, 4, 2226–2236. [Google Scholar] [CrossRef] [PubMed]
- Majidnia, E.; Ahmadian, M.; Salehi, H.; Amirpour, N. Development of an Electrospun Poly(ε-Caprolactone)/Collagen-Based Human Amniotic Membrane Powder Scaffold for Culturing Retinal Pigment Epithelial Cells. Sci. Rep. 2022, 12, 6469. [Google Scholar] [CrossRef]
- Murphy, S.V.; Skardal, A.; Song, L.; Sutton, K.; Haug, R.; Mack, D.L.; Jackson, J.; Soker, S.; Atala, A. Solubilized Amnion Membrane Hyaluronic Acid Hydrogel Accelerates Full-Thickness Wound Healing. Stem Cells Transl. Med. 2017, 6, 2020–2032. [Google Scholar] [CrossRef]
- Go, Y.Y.; Kim, S.E.; Cho, G.J.; Chae, S.-W.; Song, J.-J. Promotion of Osteogenic Differentiation by Amnion/Chorion Membrane Extracts. J. Appl. Biomater. Funct. Mater. 2016, 14, 171–180. [Google Scholar] [CrossRef]
- Lai, J.-Y. Photo-Cross-Linking of Amniotic Membranes for Limbal Epithelial Cell Cultivation. Mater. Sci. Eng. C Mater. Biol. Appl. 2014, 45, 313–319. [Google Scholar] [CrossRef]
- Gobinathan, S.; Zainol, S.S.; Azizi, S.F.; Iman, N.M.; Muniandy, R.; Hasmad, H.N.; Yusof, M.R.B.; Husain, S.; Abd Aziz, H.; Lokanathan, Y. Decellularization and Genipin Crosslinking of Amniotic Membrane Suitable for Tissue Engineering Applications. J. Biomater. Sci. Polym. Ed. 2018, 29, 2051–2067. [Google Scholar] [CrossRef]
- Pozzobon, M.; D’Agostino, S.; Roubelakis, M.G.; Cargnoni, A.; Gramignoli, R.; Wolbank, S.; Gindraux, F.; Bollini, S.; Kerdjoudj, H.; Fenelon, M.; et al. General Consensus on Multimodal Functions and Validation Analysis of Perinatal Derivatives for Regenerative Medicine Applications. Front. Bioeng. Biotechnol. 2022, 10, 961987. [Google Scholar] [CrossRef]
- Grémare, A.; Thibes, L.; Gluais, M.; Torres, Y.; Potart, D.; Da Silva, N.; Dusserre, N.; Fénelon, M.; Sentilhes, L.; Lacomme, S.; et al. Development of a Vascular Substitute Produced by Weaving Yarn Made from Human Amniotic Membrane. Biofabrication 2022, 14, 045010. [Google Scholar] [CrossRef]
- Fénelon, M.; Etchebarne, M.; Siadous, R.; Grémare, A.; Durand, M.; Sentilhes, L.; Catros, S.; Gindraux, F.; L’Heureux, N.; Fricain, J.-C. Comparison of Amniotic Membrane versus the Induced Membrane for Bone Regeneration in Long Bone Segmental Defects Using Calcium Phosphate Cement Loaded with BMP-2. Mater. Sci. Eng. C 2021, 124, 112032. [Google Scholar] [CrossRef]
- Dhawan, S.; Takiar, M.; Manocha, A.; Dhawan, R.; Malhotra, R.; Gupta, J. Functionally Graded Membrane: A Novel Approach in the Treatment of Gingival Recession Defects. J. Indian Soc. Periodontol. 2021, 25, 411–417. [Google Scholar] [CrossRef] [PubMed]
- Kesting, M.R.; Wolff, K.-D.; Mücke, T.; Demtroeder, C.; Kreutzer, K.; Schulte, M.; Jacobsen, F.; Hirsch, T.; Loeffelbein, D.J.; Steinstraesser, L. A Bioartificial Surgical Patch from Multilayered Human Amniotic Membrane-In Vivo Investigations in a Rat Model. J. Biomed. Mater. Res. B Appl. Biomater. 2009, 90, 930–938. [Google Scholar] [CrossRef] [PubMed]
- Jin, C.Z.; Park, S.R.; Choi, B.H.; Lee, K.-Y.; Kang, C.K.; Min, B.-H. Human Amniotic Membrane as a Delivery Matrix for Articular Cartilage Repair. Tissue Eng. 2007, 13, 693–702. [Google Scholar] [CrossRef]
- Hussin, I.H.; Pingguan-Murphy, B.; Osman, S.Z. The Fabrication of Human Amniotic Membrane Based Hydrogel for Cartilage Tissue Engineering Applications: A Preliminary Study. In Proceedings of the 5th Kuala Lumpur International Conference on Biomedical Engineering 2011, Kuala Lumpur, Malaysia, 20–23 June 2011; Osman, N.A.A., Abas, W.A.B.W., Wahab, A.K.A., Ting, H.-N., Eds.; Springer: Berlin/Heidelberg, Germany, 2011; Volume 35, pp. 841–844. [Google Scholar]
- Pires, A.S.; Bollini, S.; Botelho, M.F.; Lang-Olip, I.; Ponsaerts, P.; Balbi, C.; Lange-Consiglio, A.; Fénelon, M.; Mojsilović, S.; Berishvili, E.; et al. Guidelines to Analyze Preclinical Studies Using Perinatal Derivatives. Methods Protoc. 2023, 6, 45. [Google Scholar] [CrossRef] [PubMed]
- Maljaars, L.P.; Bendaoud, S.; Kastelein, A.W.; Guler, Z.; Hooijmans, C.R.; Roovers, J.-P.W.R. Application of Amniotic Membranes in Reconstructive Surgery of Internal Organs-A Systematic Review and Meta-Analysis. J. Tissue Eng. Regen. Med. 2022, 16, 1069–1090. [Google Scholar] [CrossRef]
- Toda, A.; Okabe, M.; Yoshida, T.; Nikaido, T. The Potential of Amniotic Membrane/Amnion-Derived Cells for Regeneration of Various Tissues. J. Pharmacol. Sci. 2007, 105, 215–228. [Google Scholar] [CrossRef]
- Lefebvre, S.; Adrian, F.; Moreau, P.; Gourand, L.; Dausset, J.; Berrih-Aknin, S.; Carosella, E.D.; Paul, P. Modulation of HLA-G Expression in Human Thymic and Amniotic Epithelial Cells. Hum. Immunol. 2000, 61, 1095–1101. [Google Scholar] [CrossRef]
- Hao, Y.; Ma, D.H.; Hwang, D.G.; Kim, W.S.; Zhang, F. Identification of Antiangiogenic and Antiinflammatory Proteins in Human Amniotic Membrane. Cornea 2000, 19, 348–352. [Google Scholar] [CrossRef]
- Deus, I.A.; Mano, J.F.; Custódio, C.A. Perinatal Tissues and Cells in Tissue Engineering and Regenerative Medicine. Acta Biomater. 2020, 110, 1–14. [Google Scholar] [CrossRef]
- Mamede, A.C.; Laranjo, M.; Carvalho, M.J.; Abrantes, A.M.; Pires, A.S.; Brito, A.F.; Moura, P.; Maia, C.J.; Botelho, M.F. Effect of Amniotic Membrane Proteins in Human Cancer Cell Lines: An Exploratory Study. J. Membr. Biol. 2014, 247, 357–360. [Google Scholar] [CrossRef]
- Niknejad, H.; Yazdanpanah, G. Anticancer Effects of Human Amniotic Membrane and Its Epithelial Cells. Med. Hypotheses 2014, 82, 488–489. [Google Scholar] [CrossRef] [PubMed]
- Najibpour, N.; Ahmed, M.A.A.H.; Bananzadeh, A.; Rezaianzadeh, A.; Kermani, M.R.; Gabash, K.M.; Tajali, H.; Hosseini, S.V.; Mehrabani, D. The Effect of Human Amniotic Membrane as a Covering Layer on Propylene Mesh in Decrease of Adhesion after Laparotomy in the Rabbit. Comp. Clin. Pathol. 2016, 25, 131–135. [Google Scholar] [CrossRef]
- Jirsova, K.; Jones, G.L.A. Amniotic Membrane in Ophthalmology: Properties, Preparation, Storage and Indications for Grafting-a Review. Cell Tissue Bank. 2017, 18, 193–204. [Google Scholar] [CrossRef]
- Lee, S.B.; Li, D.Q.; Tan, D.T.; Meller, D.C.; Tseng, S.C. Suppression of TGF-Beta Signaling in Both Normal Conjunctival Fibroblasts and Pterygial Body Fibroblasts by Amniotic Membrane. Curr. Eye Res. 2000, 20, 325–334. [Google Scholar] [CrossRef]
- Ricci, E.; Vanosi, G.; Lindenmair, A.; Hennerbichler, S.; Peterbauer-Scherb, A.; Wolbank, S.; Cargnoni, A.; Signoroni, P.B.; Campagnol, M.; Gabriel, C.; et al. Anti-Fibrotic Effects of Fresh and Cryopreserved Human Amniotic Membrane in a Rat Liver Fibrosis Model. Cell Tissue Bank. 2013, 14, 475–488. [Google Scholar] [CrossRef]
- Schmiedova, I.; Dembickaja, A.; Kiselakova, L.; Nowakova, B.; Slama, P. Using of Amniotic Membrane Derivatives for the Treatment of Chronic Wounds. Membranes 2021, 11, 941. [Google Scholar] [CrossRef]
- Castellanos, G.; Bernabé-García, Á.; Moraleda, J.M.; Nicolás, F.J. Amniotic Membrane Application for the Healing of Chronic Wounds and Ulcers. Placenta 2017, 59, 146–153. [Google Scholar] [CrossRef]
- Mamede, A.C.; Carvalho, M.J.; Abrantes, A.M.; Laranjo, M.; Maia, C.J.; Botelho, M.F. Amniotic Membrane: From Structure and Functions to Clinical Applications. Cell Tissue Res. 2012, 349, 447–458. [Google Scholar] [CrossRef]
- Kjaergaard, N.; Hein, M.; Hyttel, L.; Helmig, R.B.; Schønheyder, H.C.; Uldbjerg, N.; Madsen, H. Antibacterial Properties of Human Amnion and Chorion in Vitro. Eur. J. Obstet. Gynecol. Reprod. Biol. 2001, 94, 224–229. [Google Scholar] [CrossRef]
- Koob, T.J.; Lim, J.J.; Massee, M.; Zabek, N.; Rennert, R.; Gurtner, G.; Li, W.W. Angiogenic Properties of Dehydrated Human Amnion/Chorion Allografts: Therapeutic Potential for Soft Tissue Repair and Regeneration. Vasc. Cell 2014, 6, 10. [Google Scholar] [CrossRef]
- López Martínez, J.A.; Rodríguez Valiente, M.; Fuente-Mora, C.; García-Hernández, A.M.; Cánovas Sanchís, S.; Fernández Pascual, C.J. Use of Cryopreserved Human Amniotic Membrane in the Treatment of Skin Ulcers Secondary to Calciphylaxis. Dermatol. Ther. 2021, 34, e14769. [Google Scholar] [CrossRef] [PubMed]
- Fitriani, N.; Wilar, G.; Narsa, A.C.; Mohammed, A.F.A.; Wathoni, N. Application of Amniotic Membrane in Skin Regeneration. Pharmaceutics 2023, 15, 748. [Google Scholar] [CrossRef] [PubMed]
- Tsuno, H.; Arai, N.; Sakai, C.; Okabe, M.; Koike, C.; Yoshida, T.; Nikaido, T.; Noguchi, M. Intraoral Application of Hyperdry Amniotic Membrane to Surgically Exposed Bone Surface. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. 2014, 117, e83–e87. [Google Scholar] [CrossRef] [PubMed]
- Nejad, A.R.; Hamidieh, A.A.; Amirkhani, M.A.; Sisakht, M.M. Update Review on Five Top Clinical Applications of Human Amniotic Membrane in Regenerative Medicine. Placenta 2021, 103, 104–119. [Google Scholar] [CrossRef]
- Fenelon, M.; Etchebarne, M.; Siadous, R.; Grémare, A.; Durand, M.; Sentilhes, L.; Torres, Y.; Catros, S.; Gindraux, F.; L’Heureux, N.; et al. Assessment of Fresh and Preserved Amniotic Membrane for Guided Bone Regeneration in Mice. J. Biomed. Mater. Res. A 2020, 108, 2044–2056. [Google Scholar] [CrossRef]
- Fenelon, M.; Maurel, D.B.; Siadous, R.; Gremare, A.; Delmond, S.; Durand, M.; Brun, S.; Catros, S.; Gindraux, F.; L’Heureux, N.; et al. Comparison of the Impact of Preservation Methods on Amniotic Membrane Properties for Tissue Engineering Applications. Mater. Sci. Eng. C 2019, 104, 109903. [Google Scholar] [CrossRef]
- Riau, A.K.; Beuerman, R.W.; Lim, L.S.; Mehta, J.S. Preservation, Sterilization and de-Epithelialization of Human Amniotic Membrane for Use in Ocular Surface Reconstruction. Biomaterials 2010, 31, 216–225. [Google Scholar] [CrossRef]
- Niknejad, H.; Peirovi, H.; Jorjani, M.; Ahmadiani, A.; Ghanavi, J.; Seifalian, A.M. Properties of the Amniotic Membrane for Potential Use in Tissue Engineering. Eur. Cell. Mater. 2008, 15, 88–99. [Google Scholar] [CrossRef]
- Grémare, A.; Jean-Gilles, S.; Musqui, P.; Magnan, L.; Torres, Y.; Fénelon, M.; Brun, S.; Fricain, J.-C.; L’Heureux, N. Cartography of the Mechanical Properties of the Human Amniotic Membrane. J. Mech. Behav. Biomed. Mater. 2019, 99, 18–26. [Google Scholar] [CrossRef]
- Massie, I.; Kureshi, A.K.; Schrader, S.; Shortt, A.J.; Daniels, J.T. Optimization of Optical and Mechanical Properties of Real Architecture for 3-Dimensional Tissue Equivalents: Towards Treatment of Limbal Epithelial Stem Cell Deficiency. Acta Biomater. 2015, 24, 241–250. [Google Scholar] [CrossRef]
- Swim, M.M.; Albertario, A.; Iacobazzi, D.; Caputo, M.; Ghorbel, M.T. Amnion-Based Scaffold with Enhanced Strength and Biocompatibility for In Vivo Vascular Repair. Tissue Eng. Part A 2019, 25, 603–619. [Google Scholar] [CrossRef] [PubMed]
- Maljaars, L.P.; Guler, Z.; Roovers, J.-P.W.R.; Bezuidenhout, D. Mechanical Reinforcement of Amniotic Membranes for Vesicovaginal Fistula Repair. J. Mech. Behav. Biomed. Mater. 2023, 139, 105680. [Google Scholar] [CrossRef] [PubMed]
- Laranjo, M. Preservation of Amniotic Membrane. In Amniotic Membrane: Origin, Characterization and Medical Applications; Mamede, A.C., Botelho, M.F., Eds.; Springer: Dordrecht, The Netherlands, 2015; pp. 209–230. ISBN 978-94-017-9975-1. [Google Scholar]
- Gindraux, F.; Laurent, R.; Nicod, L.; de Billy, B.; Meyer, C.; Zwetyenga, N.; Wajszczak, L.; Garbuio, P.; Obert, L. Human Amniotic Membrane: Clinical Uses, Patents and Marketed Products. Recent Pat. Regen. Med. 2013, 3, 193–214. [Google Scholar] [CrossRef]
- Gholipourmalekabadi, M.; Mozafari, M.; Salehi, M.; Seifalian, A.; Bandehpour, M.; Ghanbarian, H.; Urbanska, A.M.; Sameni, M.; Samadikuchaksaraei, A.; Seifalian, A.M. Development of a Cost-Effective and Simple Protocol for Decellularization and Preservation of Human Amniotic Membrane as a Soft Tissue Replacement and Delivery System for Bone Marrow Stromal Cells. Adv. Healthc. Mater. 2015, 4, 918–926. [Google Scholar] [CrossRef] [PubMed]
- Porzionato, A.; Stocco, E.; Barbon, S.; Grandi, F.; Macchi, V.; De Caro, R. Tissue-Engineered Grafts from Human Decellularized Extracellular Matrices: A Systematic Review and Future Perspectives. Int. J. Mol. Sci. 2018, 19, 4117. [Google Scholar] [CrossRef]
- Shakouri-Motlagh, A.; Khanabdali, R.; Heath, D.E.; Kalionis, B. The Application of Decellularized Human Term Fetal Membranes in Tissue Engineering and Regenerative Medicine (TERM). Placenta 2017, 59, 124–130. [Google Scholar] [CrossRef]
- Fénelon, M.; Chassande, O.; Kalisky, J.; Gindraux, F.; Brun, S.; Bareille, R.; Ivanovic, Z.; Fricain, J.-C.; Boiziau, C. Human Amniotic Membrane for Guided Bone Regeneration of Calvarial Defects in Mice. J. Mater. Sci. Mater. Med. 2018, 29, 78. [Google Scholar] [CrossRef]
- Rodríguez-Ares, M.T.; López-Valladares, M.J.; Touriño, R.; Vieites, B.; Gude, F.; Silva, M.T.; Couceiro, J. Effects of Lyophilization on Human Amniotic Membrane. Acta Ophthalmol. 2009, 87, 396–403. [Google Scholar] [CrossRef]
- Figueiredo, G.S.; Bojic, S.; Rooney, P.; Wilshaw, S.-P.; Connon, C.J.; Gouveia, R.M.; Paterson, C.; Lepert, G.; Mudhar, H.S.; Figueiredo, F.C.; et al. Gamma-Irradiated Human Amniotic Membrane Decellularised with Sodium Dodecyl Sulfate Is a More Efficient Substrate for the Ex Vivo Expansion of Limbal Stem Cells. Acta Biomater. 2017, 61, 124–133. [Google Scholar] [CrossRef]
- Lim, L.S.; Poh, R.W.Y.; Riau, A.K.; Beuerman, R.W.; Tan, D.; Mehta, J.S. Biological and Ultrastructural Properties of Acelagraft, a Freeze-Dried γ-Irradiated Human Amniotic Membrane. Arch. Ophthalmol. 2010, 128, 1303–1310. [Google Scholar] [CrossRef]
- Paolin, A.; Trojan, D.; Leonardi, A.; Mellone, S.; Volpe, A.; Orlandi, A.; Cogliati, E. Cytokine Expression and Ultrastructural Alterations in Fresh-Frozen, Freeze-Dried and γ-Irradiated Human Amniotic Membranes. Cell Tissue Bank. 2016, 17, 399–406. [Google Scholar] [CrossRef] [PubMed]
- Von Versen-Höynck, F.; Syring, C.; Bachmann, S.; Möller, D.E. The Influence of Different Preservation and Sterilisation Steps on the Histological Properties of Amnion Allografts--Light and Scanning Electron Microscopic Studies. Cell Tissue Bank. 2004, 5, 45–56. [Google Scholar] [CrossRef] [PubMed]
- Riccio, M.; Marchesini, A.; Pugliese, P.; De Francesco, F. Nerve Repair and Regeneration: Biological Tubulization Limits and Future Perspectives. J. Cell. Physiol. 2019, 234, 3362–3375. [Google Scholar] [CrossRef]
- Sakuragawa, N.; Elwan, M.A.; Uchida, S.; Fujii, T.; Kawashima, K. Non-Neuronal Neurotransmitters and Neurotrophic Factors in Amniotic Epithelial Cells: Expression and Function in Humans and Monkey. Jpn. J. Pharmacol. 2001, 85, 20–23. [Google Scholar] [CrossRef] [PubMed]
- Mohammad, J.; Shenaq, J.; Rabinovsky, E.; Shenaq, S. Modulation of Peripheral Nerve Regeneration: A Tissue-Engineering Approach. The Role of Amnion Tube Nerve Conduit across a 1-Centimeter Nerve Gap. Plast. Reconstr. Surg. 2000, 105, 660–666. [Google Scholar] [CrossRef] [PubMed]
- Mligiliche, N.; Endo, K.; Okamoto, K.; Fujimoto, E.; Ide, C. Extracellular Matrix of Human Amnion Manufactured into Tubes as Conduits for Peripheral Nerve Regeneration. J. Biomed. Mater. Res. 2002, 63, 591–600. [Google Scholar] [CrossRef] [PubMed]
- Ozgenel, G.Y.; Fílíz, G. Combined Application of Human Amniotic Membrane Wrapping and Hyaluronic Acid Injection in Epineurectomized Rat Sciatic Nerve. J. Reconstr. Microsurg. 2004, 20, 153–157. [Google Scholar] [CrossRef]
- O’Neill, A.C.; Randolph, M.A.; Bujold, K.E.; Kochevar, I.E.; Redmond, R.W.; Winograd, J.M. Preparation and Integration of Human Amnion Nerve Conduits Using a Light-Activated Technique. Plast. Reconstr. Surg. 2009, 124, 428–437. [Google Scholar] [CrossRef]
- Meng, H.; Li, M.; You, F.; Du, J.; Luo, Z. Assessment of Processed Human Amniotic Membrane as a Protective Barrier in Rat Model of Sciatic Nerve Injury. Neurosci. Lett. 2011, 496, 48–53. [Google Scholar] [CrossRef]
- Fairbairn, N.G.; Ng-Glazier, J.; Meppelink, A.M.; Randolph, M.A.; Valerio, I.L.; Fleming, M.E.; Winograd, J.M.; Redmond, R.W. Light-Activated Sealing of Nerve Graft Coaptation Sites Improves Outcome Following Large Gap Peripheral Nerve Injury. Plast. Reconstr. Surg. 2015, 136, 739–750. [Google Scholar] [CrossRef]
- Razdan, S.; Bajpai, R.R.; Razdan, S.; Sanchez, M.A. A Matched and Controlled Longitudinal Cohort Study of Dehydrated Human Amniotic Membrane Allograft Sheet Used as a Wraparound Nerve Bundles in Robotic-Assisted Laparoscopic Radical Prostatectomy: A Puissant Adjunct for Enhanced Potency Outcomes. J. Robot. Surg. 2019, 13, 475–481. [Google Scholar] [CrossRef] [PubMed]
- Bai, J.; Liu, C.; Kong, L.; Tian, S.; Yu, K.; Tian, D. Electrospun Polycaprolactone (PCL)-Amnion Nanofibrous Membrane Promotes Nerve Regeneration and Prevents Fibrosis in a Rat Sciatic Nerve Transection Model. Front. Surg. 2022, 9, 842540. [Google Scholar] [CrossRef] [PubMed]
- Bourgeois, M.; Loisel, F.; Obert, L.; Pluvy, I.; Gindraux, F. Can the Amniotic Membrane Be Used to Treat Peripheral Nerve Defects? A Review of Literature. Hand Surg. Rehabil. 2019, 38, 223–232. [Google Scholar] [CrossRef]
- Gulameabasse, S.; Gindraux, F.; Catros, S.; Fricain, J.-C.; Fenelon, M. Chorion and Amnion/Chorion Membranes in Oral and Periodontal Surgery: A Systematic Review. J. Biomed. Mater. Res. B Appl. Biomater. 2020, 109, 1216–1229. [Google Scholar] [CrossRef] [PubMed]
- Hassan, M.; Prakasam, S.; Bain, C.; Ghoneima, A.; Liu, S.S. A Randomized Split-Mouth Clinical Trial on Effectiveness of Amnion-Chorion Membranes in Alveolar Ridge Preservation: A Clinical, Radiologic, and Morphometric Study. Int. J. Oral Maxillofac. Implant. 2017, 32, 1389–1398. [Google Scholar] [CrossRef]
- Arifin, N.; Sudin, I.; Ngadiman, N.H.A.; Ishak, M.S.A. A Comprehensive Review of Biopolymer Fabrication in Additive Manufacturing Processing for 3D-Tissue-Engineering Scaffolds. Polymers 2022, 14, 2119. [Google Scholar] [CrossRef]
- Zadpoor, A.A.; Malda, J. Additive Manufacturing of Biomaterials, Tissues, and Organs. Ann. Biomed. Eng. 2017, 45, 1–11. [Google Scholar] [CrossRef]
- Sarabia-Vallejos, M.A.; Rodríguez-Umanzor, F.E.; González-Henríquez, C.M.; Rodríguez-Hernández, J. Innovation in Additive Manufacturing Using Polymers: A Survey on the Technological and Material Developments. Polymers 2022, 14, 1351. [Google Scholar] [CrossRef]
- Nath, S.D.; Nilufar, S. An Overview of Additive Manufacturing of Polymers and Associated Composites. Polymers 2020, 12, 2719. [Google Scholar] [CrossRef]
- Mirzaali, M.J.; Moosabeiki, V.; Rajaai, S.M.; Zhou, J.; Zadpoor, A.A. Additive Manufacturing of Biomaterials—Design Principles and Their Implementation. Materials 2022, 15, 5457. [Google Scholar] [CrossRef]
- Smith, J.A.; Mele, E. Electrospinning and Additive Manufacturing: Adding Three-Dimensionality to Electrospun Scaffolds for Tissue Engineering. Front. Bioeng. Biotechnol. 2021, 9, 674738. [Google Scholar] [CrossRef]
- Liu, C.; Tian, S.; Bai, J.; Yu, K.; Liu, L.; Liu, G.; Dong, R.; Tian, D. Regulation of ERK1/2 and SMAD2/3 Pathways by Using Multi-Layered Electrospun PCL-Amnion Nanofibrous Membranes for the Prevention of Post-Surgical Tendon Adhesion. Int. J. Nanomed. 2020, 15, 927–942. [Google Scholar] [CrossRef]
- Adamowicz, J.; Pokrywczyńska, M.; Tworkiewicz, J.; Kowalczyk, T.; van Breda, S.V.; Tyloch, D.; Kloskowski, T.; Bodnar, M.; Skopinska-Wisniewska, J.; Marszałek, A.; et al. New Amniotic Membrane Based Biocomposite for Future Application in Reconstructive Urology. PLoS ONE 2016, 11, e0146012. [Google Scholar] [CrossRef] [PubMed]
- Dong, R.; Liu, C.; Tian, S.; Bai, J.; Yu, K.; Liu, L.; Tian, D. Electrospun Polycaprolactone (PCL)-Amnion Nanofibrous Membrane Prevents Adhesions and Promotes Nerve Repair in a Rat Model of Sciatic Nerve Compression. PLoS ONE 2020, 15, e0244301. [Google Scholar] [CrossRef] [PubMed]
- Xue, J.; Wu, T.; Dai, Y.; Xia, Y. Electrospinning and Electrospun Nanofibers: Methods, Materials, and Applications. Chem. Rev. 2019, 119, 5298–5415. [Google Scholar] [CrossRef] [PubMed]
- Hadipour, A.; Bayati, V.; Rashno, M.; Orazizadeh, M. Aligned Poly(ε-Caprolactone) Nanofibers Superimposed on Decellularized Human Amniotic Membrane Promoted Myogenic Differentiation of Adipose Derived Stem Cells. Cell J. 2021, 23, 603–611. [Google Scholar] [CrossRef] [PubMed]
- Nazari, H.; Heirani-Tabasi, A.; Esmaeili, E.; Kajbafzadeh, A.-M.; Hassannejad, Z.; Boroomand, S.; Shahsavari Alavijeh, M.H.; Mishan, M.A.; Ahmadi Tafti, S.H.; Warkiani, M.E.; et al. Decellularized Human Amniotic Membrane Reinforced by MoS2-Polycaprolactone Nanofibers, a Novel Conductive Scaffold for Cardiac Tissue Engineering. J. Biomater. Appl. 2022, 36, 1527–1539. [Google Scholar] [CrossRef] [PubMed]
- Hasmad, H.; Yusof, M.R.; Mohd Razi, Z.R.; Hj Idrus, R.B.; Chowdhury, S.R. Human Amniotic Membrane with Aligned Electrospun Fiber as Scaffold for Aligned Tissue Regeneration. Tissue Eng. Part C Methods 2018, 24, 368–378. [Google Scholar] [CrossRef]
- Hasmad, H.N.; Bt Hj Idrus, R.; Sulaiman, N.; Lokanathan, Y. Electrospun Fiber-Coated Human Amniotic Membrane: A Potential Angioinductive Scaffold for Ischemic Tissue Repair. Int. J. Mol. Sci. 2022, 23, 1743. [Google Scholar] [CrossRef]
- Gholipourmalekabadi, M.; Seifalian, A.M.; Urbanska, A.M.; Omrani, M.D.; Hardy, J.G.; Madjd, Z.; Hashemi, S.M.; Ghanbarian, H.; Brouki Milan, P.; Mozafari, M.; et al. 3D Protein-Based Bilayer Artificial Skin for the Guided Scarless Healing of Third-Degree Burn Wounds in Vivo. Biomacromolecules 2018, 19, 2409–2422. [Google Scholar] [CrossRef]
- Gholipourmalekabadi, M.; Samadikuchaksaraei, A.; Seifalian, A.M.; Urbanska, A.M.; Ghanbarian, H.; Hardy, J.G.; Omrani, M.D.; Mozafari, M.; Reis, R.L.; Kundu, S.C. Silk Fibroin/Amniotic Membrane 3D Bi-Layered Artificial Skin. Biomed. Mater. Bristol Engl. 2018, 13, 035003. [Google Scholar] [CrossRef] [PubMed]
- Gholipourmalekabadi, M.; Khosravimelal, S.; Nokhbedehghan, Z.; Sameni, M.; Jajarmi, V.; Urbanska, A.M.; Mirzaei, H.; Salimi, M.; Chauhan, N.P.S.; Mobaraki, M.; et al. Modulation of Hypertrophic Scar Formation Using Amniotic Membrane/Electrospun Silk Fibroin Bilayer Membrane in a Rabbit Ear Model. ACS Biomater. Sci. Eng. 2019, 5, 1487–1496. [Google Scholar] [CrossRef] [PubMed]
- Arasteh, S.; Kazemnejad, S.; Khanjani, S.; Heidari-Vala, H.; Akhondi, M.M.; Mobini, S. Fabrication and Characterization of Nano-Fibrous Bilayer Composite for Skin Regeneration Application. Methods 2016, 99, 3–12. [Google Scholar] [CrossRef]
- Fard, M.; Akhavan-Tavakoli, M.; Khanjani, S.; Zare, S.; Edalatkhah, H.; Arasteh, S.; Mehrabani, D.; Zarnani, A.-H.; Kazemnejad, S.; Shirazi, R. Bilayer Amniotic Membrane/Nano-Fibrous Fibroin Scaffold Promotes Differentiation Capability of Menstrual Blood Stem Cells into Keratinocyte-Like Cells. Mol. Biotechnol. 2018, 60, 100–110. [Google Scholar] [CrossRef] [PubMed]
- Liu, H.; Zhou, Z.; Lin, H.; Wu, J.; Ginn, B.; Choi, J.S.; Jiang, X.; Chung, L.; Elisseeff, J.H.; Yiu, S.; et al. Synthetic Nanofiber-Reinforced Amniotic Membrane via Interfacial Bonding. ACS Appl. Mater. Interfaces 2018, 10, 14559–14569. [Google Scholar] [CrossRef]
- Zhou, Z.; Long, D.; Hsu, C.-C.; Liu, H.; Chen, L.; Slavin, B.; Lin, H.; Li, X.; Tang, J.; Yiu, S.; et al. Nanofiber-Reinforced Decellularized Amniotic Membrane Improves Limbal Stem Cell Transplantation in a Rabbit Model of Corneal Epithelial Defect. Acta Biomater. 2019, 97, 310–320. [Google Scholar] [CrossRef]
- Liu, J.; Chen, D.; Zhu, X.; Liu, N.; Zhang, H.; Tang, R.; Liu, Z. Development of a Decellularized Human Amniotic Membrane-Based Electrospun Vascular Graft Capable of Rapid Remodeling for Small-Diameter Vascular Applications. Acta Biomater. 2022, 152, 144–156. [Google Scholar] [CrossRef]
- Garot, C.; Bettega, G.; Picart, C. Additive Manufacturing of Material Scaffolds for Bone Regeneration: Toward Application in the Clinics. Adv. Funct. Mater. 2021, 31, 2006967. [Google Scholar] [CrossRef]
- Koob, T.J.; Lim, J.J.; Zabek, N.; Massee, M. Cytokines in Single Layer Amnion Allografts Compared to Multilayer Amnion/Chorion Allografts for Wound Healing. J. Biomed. Mater. Res. B Appl. Biomater. 2015, 103, 1133–1140. [Google Scholar] [CrossRef]
- Zare-Bidaki, M.; Sadrinia, S.; Erfani, S.; Afkar, E.; Ghanbarzade, N. Antimicrobial Properties of Amniotic and Chorionic Membranes: A Comparative Study of Two Human Fetal Sacs. J. Reprod. Infertil. 2017, 18, 218–224. [Google Scholar]
- Romero-Araya, P.; Pino, V.; Nenen, A.; Cárdenas, V.; Pavicic, F.; Ehrenfeld, P.; Serandour, G.; Lisoni, J.G.; Moreno-Villoslada, I.; Flores, M.E. Combining Materials Obtained by 3D-Printing and Electrospinning from Commercial Polylactide Filament to Produce Biocompatible Composites. Polymers 2021, 13, 3806. [Google Scholar] [CrossRef] [PubMed]
- Kim, H.-W.; Lee, H.-H.; Knowles, J.C. Electrospinning Biomedical Nanocomposite Fibers of Hydroxyapatite/Poly(Lactic Acid) for Bone Regeneration. J. Biomed. Mater. Res. A 2006, 79, 643–649. [Google Scholar] [CrossRef] [PubMed]
- Kozior, T.; Mamun, A.; Trabelsi, M.; Wortmann, M.; Lilia, S.; Ehrmann, A. Electrospinning on 3D Printed Polymers for Mechanically Stabilized Filter Composites. Polymers 2019, 11, 2034. [Google Scholar] [CrossRef] [PubMed]
References | Electrospun Secondary Material | Applied Voltage | Polymer Flow Rate | Deposition Distance | Post-Treatment/Sterilization Process | Targeted Applications |
---|---|---|---|---|---|---|
Hadipour et al., 2021 [88] | PCL | 22 kV | 1 mL/h | 16 cm | Disinfection via 70% v/v alcohol/water solution (70:30) for 1 h and rinsed with culture medium | Muscle tissue engineering |
Nazari et al., 2022 [89] | PCL ± MoS2 | 20 kV | 0.3 mL/h | 20 cm | Sterilized using 70% filtered ethanol for 2 h and UV radiation for 20 min | Cardiac tissue engineering |
Hasmad et al., 2018 [90] | PLGA | 15 kV | 0.3 mL/h | 15 cm | Air-dried + UV-irradiated for 30 min | Aligned tissue regeneration |
Hasmad et al., 2022 [91] | 7.5 kV | Air-dried + UV-irradiated for 40 min | Ischemic tissues | |||
Gholipourmalekabadi et al., 2018a [92] | Silk fibroin | 18 kV | 0.3 mL/h | 15 cm | Treatment 70% ethanol for 1 h and subsequently dried under vacuum before storage at 4 °C | Skin substitute |
Gholipourmalekabadi et al., 2018b [93] | ||||||
Gholipourmalekabadi et al., 2019 [94] | ||||||
Arasteh et al., 2016 [95] | Silk fibroin | 15–20 kV | 0.2 mL/min | 8–18 cm | Incubation in methanol for 1 h, distilled water rinse, freeze-dried, and stored at −20 °C | Skin wound healing |
Fard et al., 2017 [96] | 18 kV | 8 cm | Incubation in methanol for 1 h, distilled water rinse and air-dried | |||
Liu et al., 2018 [97] | PLGA | 6.8 kV | 0.5 mL/h | NR | Freeze-dried and then stored at −20 °C | Limbal stem cell deficiency |
PLA | 16 kV | |||||
PCL | 12 kV | 2.5 mL/h | ||||
Zhou et al., 2019 [98] | ||||||
Liu et al., 2022 [99] | PCL + silk fibroin | 18–22 kV | 1.2 mL/h | 15 cm | NR | Vascular graft |
Liu et al., 2020 [84] | PCL | 13 kV | 1.0 mL/h | 15 cm | Air-dried | Tendon adhesion |
Dong et al., 2020 [86] | Air-dried + UV radiations | Nerve injuries | ||||
Bai et al., 2022 [74] | Air-dried + sterilized by cobalt 60 irradiation | Nerve injuries | ||||
Adamowicz et al., 2016 [85] | PLCL | 15 kV | 0.500 μL/h | 20 cm | NR | Reconstructive urology |
Dhawan et al. [21] | Chitosan HA | NR | NR | NR | NR | Gingival recession |
References | Layers Number and Composition | Mechanical Testing | Main Results (Mean ± SD) |
---|---|---|---|
Hadipour et al., 2021 [88] | Bi-layer: 1-AM 2-PCL | 50 mm × 10 mm shape strips: -UTS (MPa) -Young’s modulus (MPa) | -Significant enhancement of UTS for both aligned (0.41 ± 0.107) and random (0.26 ± 0.116) AM-PCL compared to AM (0.16 ± 0.035) (MPa) -Similar tensile strength of both aligned and random AM-PCL and AM -Significant enhancement of Young’s modulus for both aligned (2.48 ± 0.216) and random (1.34 ± 0.207) AM-PCL compared to AM (0.976 ± 0.028) (MPa) |
Nazari et al., 2022 [89] | Bi-layer: 1-AM 2-PCL Or 1-AM 2-PCL-MoS2 | 30 mm × 10 mm shape strips: -UTS (MPa) -Young’s modulus (MPa) -Strain at the breakpoint (%) | -UTS: 1.87 ± 0.16 MPa (AM), 3.14 ± 0.11 (AM-PCL) and 4.33 ± 0.23 MPa (AM-PCL-MoS2) -Young’s modulus: 45.95 (AM), 47.21 (AM-PCL) and 49.87 MPa (AM-PCL-MoS2) -Fracture point: 4.87% (AM), 6.46% (AM-PCL) and 9.39% (AM-PCL-MoS2) |
Hasmad et al., 2018 [90] | Bi-layer: 1-AM 2-PLGA | 3 mm × 10 mm shape strips: -UTS (MPa) -Young’s modulus (MPa) | -No significant difference in the UTS between AM and AM-PLGA scaffolds (in dry or wet conditions) -No significant difference in Young’s modulus between AM and AM-PLGA scaffolds (in dry or wet conditions) -Significant reduction in Young’s modulus with wet AM and AM-PLGA scaffolds compared with dry AM and AM-PLGA scaffolds |
Gholipourmalekabadi et al., 2018a [92] | Bi-layer: 1-AM 2-Silk fibroin | 20 mm × 10 mm shape strips: -Maximum load value (N) -Suture retention strength (mN) -Strain deflection at break (mm) | -Significant enhancement of maximum load value for AM–silk fibroin (1.9 ± 0.18 N) compared to AM (1.3 ± 0.17 N) -Significant enhancement of suture retention strength for AM–silk fibroin (692 ± 31 mN) compared to AM (512 ± 63 mN) -Significant enhancement of strain deflection at break for AM–silk fibroin (8.5 ± 0.33 mm) compared to AM (7.3 ± 0.49 mm) |
Arasteh et al., 2016 [95] | Bi-layer: 1-AM 2-Silk fibroin | 35 mm × 12–15 mm shape strips: -UTS (MPa) -Young’s modulus (MPa) | -De-epithelialization significantly increased the UTS and Young’s modulus of AM from 16.14 MPa and 68.46 MPa to 25.69 MPa and 108.03 MPa, respectively. -No significant difference in the UTS between AM and AM–silk fibroin -No significant difference in Young’s modulus between AM and AM–silk fibroin |
Liu et al., 2018 [97] | Bi-layer: 1-AM 2-PCL Or 1-AM 2-PLA Or 1-AM 2-PLGA | 10 mm × 10 mm shape strips: -UTS (MPa) -Elastic modulus (MPa) -Strain to failure (%) -Toughness 20 mm × 10 mm shape strips: -Suture retention strength (mN) | -Significant enhancement of UTS for the three composite membranes compared to AM alone -Significant enhancement of elastic modulus for the three composite membranes compared to AM alone -Significant enhancement of strain to failure with PCL-AM membrane compared to AM -Significant enhancement of toughness for the three composite membranes compared to AM alone -Significant enhancement of suture retention strength for the three composite membranes compared to AM alone |
Liu et al., 2020 [84] | Three-layer: 1-PCL 2-AM 3-PCL | 50.0 × 5.0 mm2 shape strips: -UTS (MPa) -Elastic modulus (MPa) -Strain to failure (%) | -Significant enhancement of UTS, elastic modulus, and strain to failure with the composite membrane compared to AM alone |
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Fenelon, M.; Galvez, P.; Kalbermatten, D.; Scolozzi, P.; Madduri, S. Emerging Strategies for the Biofabrication of Multilayer Composite Amniotic Membranes for Biomedical Applications. Int. J. Mol. Sci. 2023, 24, 14424. https://doi.org/10.3390/ijms241914424
Fenelon M, Galvez P, Kalbermatten D, Scolozzi P, Madduri S. Emerging Strategies for the Biofabrication of Multilayer Composite Amniotic Membranes for Biomedical Applications. International Journal of Molecular Sciences. 2023; 24(19):14424. https://doi.org/10.3390/ijms241914424
Chicago/Turabian StyleFenelon, Mathilde, Paul Galvez, Daniel Kalbermatten, Paolo Scolozzi, and Srinivas Madduri. 2023. "Emerging Strategies for the Biofabrication of Multilayer Composite Amniotic Membranes for Biomedical Applications" International Journal of Molecular Sciences 24, no. 19: 14424. https://doi.org/10.3390/ijms241914424