A Review on Silver Nanoparticles Based Biomaterials for Bone Tissue Engineering and Medical Applications

Nasmi Herlina Sari; Muhammad Zaidan Fadhlurrohman Rivlan; Suteja Suteja; Hamsu Kadriyan; Sentil Muthu Kumar Thiagamani

doi:10.22146/ijc.92830

A Review on Silver Nanoparticles Based Biomaterials for Bone Tissue Engineering and Medical Applications

https://doi.org/10.22146/ijc.92830

Nasmi Herlina Sari^(1*), Muhammad Zaidan Fadhlurrohman Rivlan⁽²⁾, Suteja Suteja⁽³⁾, Hamsu Kadriyan⁽⁴⁾, Sentil Muthu Kumar Thiagamani⁽⁵⁾

(1) Department of Mechanical Engineering, Faculty of Engineering, Universitas Mataram, Jl. Majapahit No. 62, Mataram 83115, Indonesia
(2) Faculty of Medical, Universitas Mataram, Jl. Majapahit No. 62, Mataram 83115, Indonesia
(3) Department of Mechanical Engineering, Faculty of Engineering, Universitas Mataram, Jl. Majapahit No. 62, Mataram 83115, Indonesia
(4) Faculty of Medical, Universitas Mataram, Jl. Majapahit No. 62, Mataram 83115, Indonesia
(5) Department of Mechanical Engineering, Kalasalingam Academy of Research and Education, Srivilliputhur 626126, India
(*) Corresponding Author

Abstract

Silver nanoparticles (AgNPs) are being studied extensively as nanostructures for novel and enhanced biomedical applications. Nanoparticles in bone grafts have been shown to speed up fracture healing by providing a finer structure for bone tissue engineering. They are known to have excellent antimicrobial properties due to their high surface-to-volume ratio and small particle size, without affecting the material's mechanical properties. AgNPs' distinct property makes them the preferred filler in a wide range of biomaterials, where they play an important role in enhancing properties. AgNP-containing biomaterials can be easily tailored to meet specific requirements in the development of bone tissue. Adjusting size, shape, composition, and surface charge can enhance their effectiveness in interacting with bone cells, promoting cell attachment, and delivering growth factors. Using AgNP-based biomaterials can help prevent or reduce the formation of biofilms. The utilization of these materials in bone tissue engineering has demonstrated potential in treating musculoskeletal conditions and bone traumas. They are versatile for various applications such as bone implants, scaffolds, wound dressings, and antibiotic delivery systems. This review will cover several special topics, including silver-based biomaterials, toxic properties, morphology and mechanical properties of silver-based biomaterials, and applications of silver-based biomaterials in medical applications.

Keywords

antimicrobial properties; bone tissue engineering; biomaterials; nano silver particles; medical applications

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References

[1] Diba, M., Koons, G.L., Bedell, M.L., and Mikos, A.G., 2021, 3D Printed colloidal biomaterials based on photo-reactive gelatin nanoparticles, Biomaterials, 274, 120871.

[2] Miao, S., Castro, N., Nowicki, M., Xia, L., Cui, H., Zhou, X., Zhu, W., Lee, S., Sarkar, K., Vozzi, G., Tabata, Y., Fisher, J., and Zhang, L.G., 2017, 4D Printing of polymeric materials for tissue and organ regeneration, Mater. Today, 20 (10), 577–591.

[3] Campos, F., Bonhome-Espinosa, A.B., Carmona, R., Durán, J.D.G., Kuzhir, P., Alaminos, M., López-López, M.T., Rodriguez, I.A., and Carriel, V., 2021, In vivo time-course biocompatibility assessment of biomagnetic nanoparticles-based biomaterials for tissue engineering applications, Mater. Sci. Eng., C, 118, 111476.

[4] Zhang, B., Li, S., Zhang, Z., Meng, Z., He, J., Ramakrishna, S., and Zhang, C., 2023, Intelligent biomaterials for micro and nanoscale 3D printing, Curr. Opin. Biomed. Eng., 26, 100454.

[5] Noronha, V.T., Paula, A.J., Durán, G., Galembeck, A., Cogo-Müller, K., Franz-Montan, M., and Durán, N., 2017, Silver nanoparticles in dentistry, Dent. Mater., 33 (10), 1110–1126.

[6] Radha Pathania, A., Doda, S., Sharma, S., and Kundu, A., 2023, An overview of synthesis and applications of silver nano-particles, Mater. Today: Proc., In Press, Corrected Proof.

[7] Ranjani, S., Matheen, A., Antony Jenish, A., and Hemalatha, S., 2021, Nanotechnology derived natural poly bio-silver nanoparticles as a potential alternate biomaterial to protect against human pathogens, Mater. Lett., 304, 130555.

[8] Masson, A., Weill, P., Preudhomme, R., Boutros, M., Veyssière, A., and Bénateau, H., 2022, Retrospective study of long-term hard and soft tissue stability after advancement genioplasty with the use of rigid osteosynthesis, J. Stomatol. Oral Maxillofac. Surg., 123 (5), 581–586.

[9] Cavalier, E., Eastell, R., Jørgensen, N.R., Makris, K., Vasikaran, R., and Morris, H.A., 2018, “Bone Turnover Markers” in Encyclopedia of Endocrine Diseases, Eds. Huhtaniemi, I., and Martini, L., Academic Press, Oxford, UK, 116–127.

[10] Cao, Z., Bian, Y., Hu, T., Yang, Y., Cui, Z., Wang, T., Yang, S., Weng, X., Liang, R., and Tan, C., 2023, Recent advances in two-dimensional nanomaterials for bone tissue engineering, J. Materiomics, 9 (5), 930–958.

[11] Cramer, M.C., D'Angelo, W.A., Dewey, M.J., Manuel, A.M., Mullett, S.J., Wendell, S.G., Napierala, D., Jiang, P., and Badylak, S.F., 2022, Extracellular vesicles present in bone, blood and extracellular matrix have distinctive characteristics and biologic roles, J. Immunol. Regener. Med., 18, 100066.

[12] Doan, P.L., Frei, A.C., Piryani, S.O., Szalewski, N., Fan, E., and Himburg, H.A., 2023, Cord blood–derived endothelial progenitor cells promote in vivo regeneration of human hematopoietic bone marrow, Int. J. Radiat. Oncol., Biol., Phys., 116 (5), 1163–1174.

[13] Entz, L., Falgayrac, G., Chauveau, C., Pasquier, G., and Lucas, S., 2022, The extracellular matrix of human bone marrow adipocytes and glucose concentration differentially alter mineralization quality without impairing osteoblastogenesis, Bone Rep., 17, 101622.

[14] Chen, X.D., Dusevich, V., Feng, J.Q., Manolagas, S.C., and Jilka, R.L., 2007, Extracellular matrix made by bone marrow cells facilitates expansion of marrow-derived mesenchymal progenitor cells and prevents their differentiation into osteoblasts, J. Bone Miner. Res., 22 (12), 1943–1956.

[15] Chen, J., Sun, T., You, Y., Wu, B., Wang, X., and Wu, J., 2021, Proteoglycans and glycosaminoglycans in stem cell homeostasis and bone tissue regeneration, Front. Cell Dev. Biol., 9, 760532.

[16] Yan, K., Zhang, X., Liu, Y., Cheng, J., Zhai, C., Shen, K., Liang, W., and Fan, W., 2023, 3D-Bioprinted silk fibroin-hydroxypropyl cellulose methacrylate porous scaffold with optimized performance for repairing articular cartilage defects, Mater. Des., 225, 111531.

[17] Wei, F., Liu, S., Chen, M., Tian, G., Zha, K., Yang, Z., Jiang, S., Li, M., Sui, X., Chen, Z., and Guo, Q., 2021, Host response to biomaterials for cartilage tissue engineering: Key to remodeling, Front. Bioeng. Biotechnol., 9, 664592.

[18] Ma, J., and Wu, C., 2022, Bioactive inorganic particles‐based biomaterials for skin tissue engineering, Exploration, 2 (5), 20210083.

[19] Jiang, S., Guo, W., Tian, G., Luo, X., Peng, L., Liu, S., Sui, X., Guo, Q., and Li, X., 2020, Clinical applications status of articular catilage regeneration techniques: Tissue-engineered cartilage brings new hope, Stem Cells Int., 2020, 5690252.

[20] Zhang, Q., Zhou, J., Zhi, P., Liu, L., Liu, C., Fang, A., and Zhang, Q., 2023, 3D Printing method for bone tissue engineering scaffold, Med. Novel Technol. Devices, 17, 100205.

[21] Bittner, S., Smith, B., Melchiorri, A., and Mikos, A., 2017, Fabrication of 3D-printed, bidirectional growth factor gradient scaffolds for osteochondral tissue repair, Tissue Eng., Part A, 23, S38–S39.

[22] Wang, Q., Wang, Q., and Wan, C., 2012, Preparation and evaluation of a biomimetic scaffold with porosity gradients in vitro, An. Acad. Bras. Cienc., 84 (1), 9–16.

[23] Kim, K.J., Yun, Y.H., Je, J.Y., Kim, D.H., Hwang, H.S., and Yoon, S.D., 2023, Photothermally controlled drug release of naproxen-incorporated mungbean starch/PVA biomaterials adding melanin nanoparticles, Process Biochem., 129, 268–280.

[24] Kersey, A.L., Nguyen, T.U., Nayak, B., Singh, I., and Gaharwar, A.K., 2023, Omics-based approaches to guide the design of biomaterials, Mater. Today, 64, 98–120.

[25] Sebastian, J.A., Strohm, E.M., Baranger, J., Villemain, O., Kolios, M.C., and Simmons, C.A., 2023, Assessing engineered tissues and biomaterials using ultrasound imaging: In vitro and in vivo applications, Biomaterials, 296, 122054.

[26] Rajput, A.S., Das, M., and Kapil, S., 2023, Investigation of surface characteristics on post processed additively manufactured biomaterial through magnetorheological fluid assisted finishing process, Wear, 522, 204684.

[27] Behera, A., 2022, “Biomaterials” in Advanced Materials: An Introduction to Modern Materials Science, Springer, Cham, Switzerland, 439–467.

[28] Kim, J., Heo, J.N., Do, J.Y., Chava, R.K., and Kang, M., 2019, Electrochemical synergies of heterostructured Fe₂O₃-MnO catalyst for oxygen evolution reaction in alkaline water splitting, Nanomaterials, 9 (10), 1486.

[29] Radenković, G., and Petković, D., 2018, “Metallic Biomaterials” in Biomaterials in Clinical Practice: Advances in Clinical Research and Medical, Eds. Zivic, F., Affatato, S., Trajanovic, M., Schnabelrauch, M., Grujovic, N., and Choy, K., Springer, Cham, Switzerland, 183–224.

[30] Mohan, P., Rajak, D.K., Pruncu, C.I., Behera, A., Amigó-Borrás, V., and Elshalakany, A.B., 2021, Influence of β-phase stability in elemental blended Ti-Mo and Ti-Mo-Zr alloys, Micron, 142, 102992.

[31] Su, Y., Cockerill, I., Wang, Y., Qin, Y.X., Chang, L., Zheng, Y., and Zhu, D., 2018, Zinc-based biomaterials for regeneration and therapy, Trends Biotechnol., 37 (4), 428–441.

[32] Suresh babu, J., Saravanan, A., Muthuvel, B., George, R., and Narayanan, J., 2023, Synthesis and characterization of natural biomaterial composite nanofibers for ocular drug delivery systems, OpenNano, 10, 100122.

[33] Ullah, S., and Chen, X., 2020, Fabrication, applications and challenges of natural biomaterials in tissue engineering, Appl. Mater. Today, 20, 100656.

[34] Hansen, C.J., and Primas, F., 2009, Silver Stars, Proceedings IAU Symposium, 265, 67–68.

[35] Bouadma, L., Wolff, M., and Lucet, J.C., 2012, Ventilator-associated pneumonia and its prevention, Curr. Opin. Infect. Dis., 25 (4), 395–404.

[36] Maillard, J.Y., and Hartemann, P., 2012, Silver as an antimicrobial: Facts and gaps in knowledge, Crit. Rev. Microbiol., 39 (4), 373–383.

[37] Bruna, T., Maldonado-Bravo, F., Jara, P., and Caro, N, 2021, Silver nanoparticles and their antibacterial applications, Int. J. Mol. Sci., 22 (13), 7202.

[38] Qing, Y., Cheng, L., Li, R., Liu, G., Zhang, Y., Tang, X., Wang, J., Liu, H., and Qin, Y., 2018, Potential antibacterial mechanism of silver nanoparticles and the optimization of orthopedic implants by advanced modification technologies, Int. J. Nanomed., 13, 3311–3327.

[39] Korshed, P., Li, L., Liu, Z., Mironov, A., and Wang, T., 2019, Size-dependent antibacterial activity for laser-generated silver nanoparticles, J. Interdiscip. Nanomed., 4 (1), 24–33.

[40] ASTM-E 2197-02, A standard quantitative test for determining the bactericidal, virucidal, fungicidal and sporocidal activities of liquid chemical germicides, ASTM International, West Conshohocken, PA, US.

[41] Gomaa, E.Z, 2017, Silver nanoparticles as an antimicrobial agent: A case study on Staphylococcus aureus and Escherichia coli as models for Gram-positive and Gram-negative bacteria, J. Gen. Appl. Microbiol., 63 (1), 36–43.

[42] Mousavi, A., Mashayekhan, S., Baheiraei, N., and Pourjavadi, A., 2021, Biohybrid oxidized alginate/myocardial extracellular matrix injectable hydrogels with improved electromechanical properties for cardiac tissue engineering, Int. J. Biol. Macromol., 180, 692–708.

[43] Zhang, X.F., Liu, Z.G., Shen, W., and Gurunathan, S., 2016, Silver nanoparticles: Synthesis, characterization, properties, applications, and therapeutic approaches, Int. J. Mol. Sci., 17 (9), 1534.

[44] Elsupikhe, R.F., Shameli, K., Ahmad, M.B., Ibrahim, N.A., and Zainudin, N., 2015, Green sonochemical synthesis of silver nanoparticles at varying concentrations of κ-carrageenan, Nanoscale Res. Lett., 10 (1), 302.

[45] Li, W.R., Xie, X.B., Shi, Q.S., Zeng, H.Y., Ou-Yang, Y.S., and Chen, Y.B., 2010, Antibacterial activity and mechanism of silver nanoparticles on Escherichia coli, Appl. Microbiol. Biotechnol., 85 (4), 1115–1122.

[46] Abdo, M.M., Abdel-Hamid, M.I., El-Sherbiny, I.M., El-Sherbeny, G., and Abdel-Aal, E.I., 2023, Green synthesis of AgNPs, alginate microbeads and Chlorella minutissima laden alginate microbeads for tertiary treatment of municipal waste water, Bioresour. Technol. Rep., 21, 101300.

[47] Tamimi, M., Rajabi, S., and Pezeshki-Modaress, M., 2020, Cardiac ECM/chitosan/alginate ternary scaffolds for cardiac tissue engineering application, Int. J. Biol. Macromol., 164, 389–402.

[48] Castillo-Henríquez, L., Alfaro-Aguilar, K., Ugalde-Álvarez, J., Vega-Fernández, L., Montes de Oca-Vásquez, G., and Vega-Baudrit, J.R., 2020, Green synthesis of gold and silver nanoparticles from plant extracts and their possible applications as antimicrobial agents in the agricultural area, Nanomaterials, 10 (9), 1763.

[49] Elamawi, R.M., Al-Harbi, R.E., and Hendi, A.A., 2018, Biosynthesis and characterization of silver nanoparticles using Trichoderma longibrachiatum and their effect on phytopathogenic fungi, Egypt. J. Biol. Pest Control, 28 (1), 28.

[50] Fayez, H., El-Motaleb, M.A., and Selim, A.A., 2020, Synergistic cytotoxicity of shikonin-silver nanoparticles as an opportunity for lung cancer, J. Labelled Compd. Radiopharm., 63 (1), 25–32.

[51] Ferdous, Z., and Nemmar, A., 2020, Health impact of silver nanoparticles: A review of the biodistribution and toxicity following various routes of exposure, Int. J. Mol. Sci., 21 (7), 2375.

[52] Kubo, A.L., Capjak, I., Vrček, I.V., Bondarenko, O.M., Kurvet, I., Vija, H., Ivask, A., Kasemets, K., and Kahru, A., 2018, Antimicrobial potency of differently coated 10 and 50 nm silver nanoparticles against clinically relevant bacteria Escherichia coli and Staphylococcus aureus, Colloids Surf., B, 170, 401–410.

[53] Kalaivani, R., Maruthupandy, M., Muneeswaran, T., Hameedha Beevi, A., Anand, M., Ramakritinan, C.M., and Kumaraguru, A.K., 2018, Synthesis of chitosan mediated silver nanoparticles (Ag NPs) for potential antimicrobial applications, Front. Lab. Med., 2 (1), 30–35.

[54] Tamilselvan, S., Ashokkumar, T., and Govindaraju, K., 2017, Microscopy based studies on the interaction of bio-based silver nanoparticles with Bombyx mori nuclear polyhedrosis virus, J. Virol. Methods, 242, 58–66.

[55] Bapat, R.A., Chaubal, T.V., Joshi, C.P., Bapat, P.R., Choudhury, H., Pandey, M., Gorain, B., and Kesharwani, P., 2018, An overview of application of silver nanoparticles for biomaterials in dentistry, Mater. Sci. Eng., C, 91, 881–898.

[56] Prabhu, S., and Poulose, E.K., 2012, Silver nanoparticles: Mechanism of antimicrobial action, synthesis, medical applications, and toxicity effects, Int. Nano Lett., 2 (1), 32.

[57] Dubey, P., Matai, I., Kumar, S.U., Sachdev, A., Bhushan, B., and Gopinath, P., 2015, Perturbation of cellular mechanistic system by silver nanoparticle toxicity: Cytotoxic, genotoxic and epigenetic potentials, Adv. Colloid Interface Sci., 221, 4–21.

[58] Bukhary, H.A., Zaman, U., ur Rehman, K., Alissa, M., Rizg, W.Y., Khan, D., Almehizia, A.A., Naglah, A.M., Al-Wasidi, A.S., Alharbi, A.S., Refat, M.S., and Abdelrahman, E.A., 2023, Acid protease functionalized novel silver nanoparticles (APTs-AgNPs): A new approach towards photocatalytic and biological applications, Int. J. Biol. Macromol., 242 (Part 2), 124809.

[59] Poon, T.K.C., Iyengar, K.P., and Jain, V.K., 2021, Silver nanoparticle (AgNP) technology applications in trauma and orthopaedics, J. Clin. Orthop. Trauma, 21, 101536.

[60] Sk, M.M., Das, P., Panwar, A., and Tan, L.P., 2021, Synthesis and characterization of site selective photo-crosslinkable glycidyl methacrylate functionalized gelatin-based 3D hydrogel scaffold for liver tissue engineering, Mater. Sci. Eng., C, 123, 111694.

[61] Lewis, P.L., Yan, M., Su, J., and Shah, R.N., 2018, Directing the growth and alignment of biliary epithelium within extracellular matrix hydrogels, Acta Biomater., 85, 84–93.

[62] Ghahremanzadeh, F., Alihosseini, F., and Semnani, D., 2021, Investigation and comparison of new galactosylation methods on PCL/chitosan scaffolds for enhanced liver tissue engineering, Int. J. Biol. Macromol., 174, 278–288.

[63] Sari, N.H., Suteja, S., Fudholi, A., Sutaryono, Y.A., Maskur, M., Srisuk, R., Rangappa, S.M., and Siengchin, S., 2022, Evaluation of impact, thermo-physical properties, and morphology of cornhusk fiber-reinforced polyester composites, Polym. Compos., 43 (5), 2771–2778.

[64] Niu, X., Wei, Y., Liu, Q., Yang, B., Ma, N., Li, Z., Zhao, L., Chen, W., and Huang, D., 2020, Silver-loaded microspheres reinforced chitosan scaffolds for skin tissue engineering, Eur. Polym. J., 134, 109861.

[65] Salari Joo, H., Behzadi Tayemeh, M., Abaei, H., and Johari, S.A., 2023, On how zeolitic imidazolate framework-8 reduces silver ion release and affects cytotoxicity and antimicrobial properties of AgNPs@ZIF8 nanocomposite, Colloids Surf., A, 668, 131411.

[66] Subbiah, G.K., and Gopinathan, N.M., 2018, Is silver diamine fluoride effective in preventing and arresting caries in elderly adults? A systematic review, J. Int. Soc. Prev. Community Dent., 8 (3), 191–199.

[67] Zhao, I.S., Gao, S.S., Hiraishi, N., Burrow, M.F., Duangthip, D., Mei, M.L., Lo, E.C.M., and Chu, C.H., 2018, Mechanisms of silver diamine fluoride on arresting caries: A literature review, Int. Dent. J., 68 (2), 67–76.

[68] Seifo, N., Cassie, H., Radford, J.R., and Innes, N.P.T., 2019, Silver diamine fluoride for managing carious lesions: An umbrella review, BMC Oral Health, 19 (1), 145.

[69] Burgess, J.O., and Vaghela, P.M., 2018, Silver diamine fluoride: A successful anticarious solution with limits, Adv. Dent. Res., 29 (1), 131–134.

[70] Horst, J.A., 2018, Silver fluoride as a treatment for dental caries, Adv. Dent. Res., 29 (1), 135–140.

[71] Lo, E.C.M., and Duangthip, D., 2018, “Non-restorative Approaches for Managing Cavitated Dentin Carious Lesions” in Pediatric Restorative Dentistry, Eds. Coelho Leal, S., and Takeshita, E.M., Springer International Publishing, Switzerland, 141–160.

[72] Boateng, J.S., and Catanzano, O., 2015, Advanced therapeutic dressings for effective wound healing–A review, J. Pharm. Sci., 104 (11), 3653–3680.

[73] Kim, H., Makin, I., Skiba, J., Ho, A., Housler, G., Stojadinovic, A., and Izadjoo, M., 2014, Antibacterial efficacy testing of a bioelectric wound dressing against clinical wound pathogens, Open Microbiol. J., 8, 15–21.

[74] Trieu, A., Mohamed, A., and Lynch, E., 2019, Silver diamine fluoride versus sodium fluoride for arresting dentine caries in children: A systematic review and meta-analysis, Sci. Rep., 9 (1), 2115.

[75] Seifo, N., Robertson, M., MacLean, J., Blain, K., Grosse, S., Milne, R., Seeballuck, C., and Innes, N., 2020, The use of silver diamine fluoride (SDF) in dental practice, Br. Dent. J., 228 (2), 75–81.

[76] World Health Organization, 2021, World Health Organization model list of essential medicines: 22nd list, 2021, World Health Organization, Geneva, WHO/MHP/HPS/EML/2021.02.

[77] Jalili Tabaii, M., and Emtiazi, G., 2018, Transparent nontoxic antibacterial wound dressing based on silver nanoparticle/bacterial cellulose nanocomposite synthesized in the presence of tripolyphosphate, J. Drug Delivery Sci. Technol., 44, 244–253.

[78] Yuan, Y., Ding, L., Chen, Y., Chen, G., Zhao, T., and Yu, Y., 2022, Nano-silver functionalized polysaccharides as a platform for wound dressings: A review, Int. J. Biol. Macromol., 194, 644–653.

[79] Paneysar, J.S., Barton, S., Ambre, P., and Coutinho, E., 2022, Novel temperature responsive films impregnated with silver nano particles (Ag-NPs) as potential dressings for wounds, J. Pharm. Sci., 111, (3), 810–817.

[80] Ryan, C.N.M., Pugliese, E., Shologu, N., Gaspar, D., Rooney, P., Islam, M.M., O'Riordan, A., Biggs, M.J., Griffin, M.D., and Zeugolis, D.I., 2023, The synergistic effect of physicochemical in vitro microenvironment modulators in human bone marrow stem cell cultures, Biomater. Adv., 144, 213196.

[81] Cao, Z., Bian, Y., Hu, T., Yang, Y., Cui, Z., Wang, T., Yang, S., Weng, X., Liang, R., and Tan, C., 2023, Recent advances in two-dimensional nanomaterials for bone tissue engineering, J. Materiomics, 9 (5), 930–958.

[82] Sari, N.H., Suteja, S., Rangappa, S.M., and Siengchin, S., 2023, A review on cellulose fibers from Eichornia crassipes: Synthesis, modification, properties and their composites, J. Nat. Fibers, 20 (1), 2162179.

[83] Nenen, A., Maureira, M., Neira, M., Orellana, S.L., Covarrubias, C., and Moreno-Villoslada, I., 2022, Synthesis of antibacterial silver and zinc doped nano-hydroxyapatite with potential in bone tissue engineering applications, Ceram. Int., 48 (23 Part A), 34750–34759.

[84] Dubnika, A., Loca, D., Rudovica, V., Parekh, M.B., and Berzina-Cimdina, L., 2017, Functionalized silver doped hydroxyapatite scaffolds for controlled simultaneous silver ion and drug delivery, Ceram. Int., 43 (4), 3698–3705.

[85] Hasan, A., Waibhaw, G., Saxena, V., and Pandey, L.M., 2018, Nano-biocomposite scaffolds of chitosan, carboxymethyl cellulose and silver nanoparticle modified cellulose nanowhiskers for bone tissue engineering applications, Int. J. Biol. Macromol., 111, 923–934.

[86] Vranceanu, D.M., Parau, A.C., Cotrut, C.M., Kiss, A.E., Constantin, L.R., Braic, V., and Vladescu, A., 2019, In vitro evaluation of Ag doped hydroxyapatite coatings in acellular media, Ceram. Int., 45 (8), 11050–11061.

[87] Pawłowski, L., Asim Akhtar, M., Zieliński, A., and Boccaccini, A.R., 2023, Biological properties of chitosan/Eudragit E 100 and chitosan/poly(4-vinylpyridine) coatings electrophoretically deposited on AgNPs-decorated titanium substrate, Mater. Lett., 336, 133885.

[88] Pawłowski, L., Wawrzyniak, J., Banach-Kopeć, A., Cieślik, B.M., Jurak, K., Karczewski, J., Tylingo, R., Siuzdak, K., and Zieliński, A, 2022, Antibacterial properties of laser-encapsulated titanium oxide nanotubes decorated with nanosilver and covered with chitosan/Eudragit polymers, Biomater. Adv., 138, 212950.

[89] Imashiro, C., and Shimizu, T., 2021, Review fundamental technologies and recent advances of cell-sheet-based tissue engineering, Int. J. Mol. Sci., 22 (1), 425.

[90] Nakayama, M., Toyoshima, Y., Chinen, H., Kikuchi, A., Yamato, M., and Okano, T., 2020, Water stable nanocoatings of poly(N-isopropylacrylamide)-based block copolymers on culture insert membranes for temperature-controlled cell adhesion, J. Mater. Chem. B, 8 (34), 7812–7821.

[91] Chang, H.K., Yang, D.H., Ha, M.Y., Kim, H.J., Kim, C.H., Kim, S.H., Choi, J.W., and Chun, H.J., 2022, 3D Printing of cell-laden visible light curable glycol chitosan bioink for bone tissue engineering, Carbohydr. Polym., 287, 119328.

[92] Bhowmick, A., Banerjee, S.L., Pramanik, N., Jana, P., Mitra, T., Gnanamani, A., Das, M., and Kundu, P.P., 2017, Organically modified clay supported chitosan/hydroxyapatite-zinc oxide nanocomposites with enhanced mechanical and biological properties for the application in bone tissue engineering, Int. J. Biol. Macromol., 106, 11–19.

[93] Narita, T., Shintani, Y., Ikebe, C., Kaneko, M., Campbell, N.G., Coppen, S.R., Uppal, R., Sawa, Y., Yashiro, K., and Suzuki, K., 2013, The use of scaffold-free cell sheet technique to refine mesenchymal stromal cell-based therapy for heart failure, Mol. Ther., 21 (4), 860–867.

[94] Wang, H., Sun, D., Lin, W., Fang, C., Cheng, K., Pan, Z., Wang, D., Song, Z., and Long, X., 2023, One-step fabrication of cell sheet-laden hydrogel for accelerated wound healing, Bioact. Mater., 28, 420–431.

[95] Zhao, H., Sun, J., Wu, Y., Zhang, J., and Shen, C., 2023, Promotion of skin wound healing using hypoimmunogenic epidermal cell sheets, Regener. Ther., 24, 245–255.

DOI: https://doi.org/10.22146/ijc.92830