From electricity to vitality: the emerging use of piezoelectric materials in tissue regeneration

Abstract

The unique ability of piezoelectric materials to generate electricity spontaneously has attracted widespread interest in the medical field. In addition to the ability to convert mechanical stress into electrical energy, piezoelectric materials offer the advantages of high sensitivity, stability, accuracy and low power consumption. Because of these characteristics, they are widely applied in devices such as sensors, controllers and actuators. However, piezoelectric materials also show great potential for the medical manufacturing of artificial organs and for tissue regeneration and repair applications. For example, the use of piezoelectric materials in cochlear implants, cardiac pacemakers and other equipment may help to restore body function. Moreover, recent studies have shown that electrical signals play key roles in promoting tissue regeneration. In this context, the application of electrical signals generated by piezoelectric materials in processes such as bone healing, nerve regeneration and skin repair has become a prospective strategy. By mimicking the natural bioelectrical environment, piezoelectric materials can stimulate cell proliferation, differentiation and connection, thereby accelerating the process of self-repair in the body. However, many challenges remain to be overcome before these concepts can be applied in clinical practice, including material selection, biocompatibility and equipment design. On the basis of the principle of electrical signal regulation, this article reviews the definition, mechanism of action, classification, preparation and current biomedical applications of piezoelectric materials and discusses opportunities and challenges for their future clinical translation.

Keywords

Smart materials / Piezoelectric / Tissue engineering / Scaffold / Regenerative medicine electrical stimulation

References

[1] Huang Z, Zhang Y, Liu R, Li Y, Rafique M, Midgley AC, et al. Cobalt loaded electrospun poly(epsilon-caprolactone) grafts promote antibacterial activity and vascular regeneration in a diabetic rat model. Biomaterials. 2022; 291: 121901.

[2] Zhang Y, Xu K, Zhi D, Qian M, Liu K, Shuai Q, et al. Improving vascular regeneration performance of electrospun poly(ε-Caprolactone) vascular grafts via synergistic functionalization with VE-cadherin/VEGF. Adv Fiber Mater. 2022; 4: 1685-702.

[3] Rafique M, Wei T, Sun Q, Midgley AC, Huang Z, Wang T, et al. The effect of hypoxia-mimicking responses on improving the regeneration of artificial vascular grafts. Biomaterials. 2021; 271: 120746. https://doi.org/10.1016/j.biomaterials.2021.120746.

[4] Murray RZ, West ZE, Cowin AJ, Farrugia BL. Development and use of biomaterials as wound healing therapies. Burns Trauma. 2019; 7: 2.

[5] Chorsi MT, Curry EJ, Chorsi HT, Das R, Baroody J, Purohit PK, et al. Piezoelectric biomaterials for sensors and actuators. Adv Mater. 2019; 31: e1802084.

[6] Ali F, Raza W, Li X, Gul H, Kim K. Piezoelectric energy harvesters for biomedical applications. Nano Energy. 2019; 57: 879-902.

[7] Wu Y, Ma Y, Zheng H, Ramakrishna S. Piezoelectric materials for flexible and wearable electronics: a review. Mater Des. 2021; 211: 110164. https://doi.org/10.1016/j.matdes.2021.110164.

[8] Tan P, Xi Y, Chao S, Jiang D, Liu Z, Fan Y, et al. An artificial intelligence-enhanced blood pressure monitor wristband based on piezoelectric Nanogenerator. Biosensors (Basel). 2022; 12: 234.

[9] Xue J, Zou Y, Deng Y, Li Z. Bioinspired sensor system for health care and human-machine interaction. EcoMat. 2022; 4: e12209.

[10] Sun M, Li Z, Yang C, Lv Y, Yuan L, Shang C, et al. Nanogenerator-based devices for biomedical applications. Nano Energy. 2021; 89: 106461.

[11] Jarkov V, Allan SJ, Bowen C, Khanbareh H. Piezoelectric materials and systems for tissue engineering and implantable energy harvesting devices for biomedical applications. Int Mater Rev. 2021; 67: 683-733.

[12] Chen C, Bai X, Ding Y, Lee IS. Electrical stimulation as a novel tool for regulating cell behavior in tissue engineering. Biomater Res. 2019; 23: 25.

[13] More N, Kapusetti G. Piezoelectric material-a promising approach for bone and cartilage regeneration. Med Hypotheses. 2017; 108: 10-6.

[14] Zhang Y, Xu L, Liu Z, Cui X, Xiang Z, Bai J, et al. Self-powered pulsed direct current stimulation system for enhancing osteogenesis in MC3T3-E1. Nano Energy. 2021; 85: 106009. https://doi.org/10.1016/j.nanoen.2021.106009.

[15] Kaliannagounder VK, Raj NPMJ, Unnithan AR, Park J, Park SS, Kim S-J, et al. Remotely controlled self-powering electrical stimulators for osteogenic differentiation using bone inspired bioactive piezoelectric whitlockite nanoparticles. Nano Energy. 2021; 85: 105901. https://doi.org/10.1016/j.nanoen.2021.105901.

[16] Zhang J, He X, Lin S, Chen X, Dong L, Lin J, et al. Accelerated Osteogenesis of heterogeneous electric potential gradient on CFO/P(VDF-TrFE) membranes. Adv Mater Interfaces. 2022; 9: 2102549.

[17] Zaszczynska A, Sajkiewicz P, Gradys A. Piezoelectric scaffolds as smart materials for neural tissue engineering. Polymers (Basel). 2020; 12: 161.

[18] Levin M, Selberg J, Rolandi M. Endogenous bioelectrics in development, cancer, and regeneration: drugs and bioelectronic devices as Electroceuticals for regenerative medicine. iScience. 2019; 22: 519-33.

[19] Luo R, Dai J, Zhang J, Li Z. Accelerated skin wound healing by electrical stimulation. Adv Healthc Mater. 2021; 10: e2100557.

[20] Liu Q, Lu WF, Zhai W. Toward stronger robocast calcium phosphate scaffolds for bone tissue engineering: a mini-review and meta-analysis. Biomater Adv. 2022; 134: 112578. https://doi.org/10.1016/j.msec.2021.112578.

[21] Sundelacruz S, Levin M, Kaplan DL. Role of membrane potential in the regulation of cell proliferation and differentiation. Stem Cell Rev Rep. 2009; 5: 231-46.

[22] LaGuardia JS, Shariati K, Bedar M, Ren X, Moghadam S, Huang KX, et al. Convergence of Calcium Channel regulation and Mechanotransduction in skeletal regenerative biomaterial design. Adv Healthc Mater. 2023; 12: e2301081. https://doi.org/10.1002/adhm.202301081.

[23] Takacs R, Kovacs P, Ebeid RA, Almassy J, Fodor J, Ducza L, et al. Ca(2+)-activated K(+) channels in progenitor cells of musculoskeletal tissues: a narrative review. Int J Mol Sci. 2023; 24: 6796.

[24] Wang L, Wang ZL. Advances in piezotronic transistors and piezotronics. Nano Today. 2021; 37: 101108. https://doi.org/10.1016/j.nantod.2021.101108.

[25] Wan C, Bowen CR. Multiscale-structuring of polyvinylidene fluoride for energy harvesting: the impact of molecular-, micro-and macro-structure. J Mater Chem A. 2017; 5: 3091-128.

[26] Surmenev RA, Orlova T, Chernozem RV, Ivanova AA, Bartasyte A, Mathur S, et al. Hybrid lead-free polymer-based nanocomposites with improved piezoelectric response for biomedical energy-harvesting applications: a review. Nano Energy. 2019; 62: 475-506.

[27] Shuai C, Liu G, Yang Y, Yang W, He C, Wang G, et al. Functionalized BaTiO3 enhances piezoelectric effect towards cell response of bone scaffold. Colloids Surf B Biointerfaces. 2020; 185: 110587. https://doi.org/10.1016/j.colsurfb.2019.110587.

[28] Ielo I, Calabrese G, De Luca G, Conoci S. Recent advances in hydroxyapatite-based biocomposites for bone tissue regeneration in Orthopedics. Int J Mol Sci. 2022; 23: 9721.

[29] Bhang SH, Jang WS, Han J, Yoon JK, La WG, Lee E, et al. Zinc oxide Nanorod-based piezoelectric dermal patch for wound healing. Adv Funct Mater. 2017; 27: 1603497.

[30] Blanquer A, Careta O, Anido-Varela L, Aranda A, Ibanez E, Esteve J, et al. Biocompatibility and electrical stimulation of skeletal and smooth muscle cells cultured on piezoelectric Nanogenerators. Int J Mol Sci. 2021; 23: 432.

[31] Augustine R, Dan P, Sosnik A, Kalarikkal N, Tran N, Vincent B, et al. Electrospun poly(vinylidene fluoride-trifluoroethylene)/zinc oxide nanocomposite tissue engineering scaffolds with enhanced cell adhesion and blood vessel formation. Nano Res. 2017; 10: 3358-76.

[32] Khare D, Majumdar S, Krishnamurthy S, Dubey AK. An in vivo toxicity assessment of piezoelectric sodium potassium niobate [Na(x)K(1-x)NbO(3) (x = 0.2-0.8)] nanoparticulates towards bone tissue engineering approach. Biomater Adv. 2022; 140: 213080. https://doi.org/10.1016/j.bioadv.2022.213080.

[33] Rajabi AH, Jaffe M, Arinzeh TL. Piezoelectric materials for tissue regeneration: a review. Acta Biomater. 2015; 24: 12-23.

[34] Jacob J, More N, Kalia K, Kapusetti G. Piezoelectric smart biomaterials for bone and cartilage tissue engineering. Inflamm Regen. 2018; 38: 2.

[35] Khare D, Basu B, Dubey AK. Electrical stimulation and piezoelectric biomaterials for bone tissue engineering applications. Biomaterials. 2020; 258: 120280. https://doi.org/10.1016/j.biomaterials.2020.120280.

[36] Hu P, Hu S, Huang Y, Reimers JR, Rappe AM, Li Y, et al. Bioferroelectric properties of glycine crystals. J Phys Chem Lett. 2019; 10: 1319-24.

[37] Basavalingappa V, Bera S, Xue B, O’Donnell J, Guerin S, Cazade PA, et al. Diphenylalanine-derivative peptide assemblies with increased aromaticity exhibit metal-like rigidity and high piezoelectricity. ACS Nano. 2020; 14: 7025-37.

[38] Yue X, Wang Z, Shi H, Wu R, Feng Y, Yuan L, et al. Silk fibroin-based piezoelectric nanofibrous scaffolds for rapid wound healing. Biomater Sci. 2023; 11: 5232-9.

[39] Szewczyk PK, Metwally S, Karbowniczek JE, Marzec MM, Stodolak-Zych E, Gruszczynski A, et al. Surface-potential-controlled cell proliferation and collagen mineralization on electrospun Polyvinylidene fluoride (PVDF) Fiber scaffolds for bone regeneration. ACS Biomater Sci Eng. 2019; 5: 582-93.

[40] Tai Y, Ico G, Low K, Liu J, Jariwala T, Garcia-Viramontes D, et al. Formation of 3D self-organized neuron-glial Interface derived from neural stem cells via Mechano-electrical stimulation. Adv Healthc Mater. 2021; 10: e2100806. https://doi.org/10.1002/adhm.202100806.

[41] Guo HF, Li ZS, Dong SW, Chen WJ, Deng L, Wang YF, et al. Piezoelectric PU/PVDF electrospun scaffolds for wound healing applications. Colloids Surf B Biointerfaces. 2012; 96: 29-36.

[42] Martins PM, Ribeiro S, Ribeiro C, Sencadas V, Gomes AC, Gama FM, et al. Effect of poling state and morphology of piezoelectric poly(vinylidene fluoride) membranes for skeletal muscle tissue engineering. RSC Adv. 2013; 3: 17938-44.

[43] Martins P, Lopes AC, Lanceros-Mendez S. Electroactive phases of poly(vinylidene fluoride): determination, processing and applications. Prog Polym Sci. 2014; 39: 683-706.

[44] Bai Y, Dai X, Yin Y, Wang J, Sun X, Liang W, et al. Biomimetic piezoelectric nanocomposite membranes synergistically enhance osteogenesis of deproteinized bovine bone grafts. Int J Nanomedicine. 2019;Volume 14: 3015-26.

[45] Lee YS, Collins G, Arinzeh TL. Neurite extension of primary neurons on electrospun piezoelectric scaffolds. Acta Biomater. 2011; 7: 3877-86.

[46] Fu Y, Liu L, Cheng R, Cui W. ECM decorated electrospun nanofiber for improving bone tissue regeneration. Polymers (Basel). 2018; 10: 272.

[47] Zhang K, Zheng H, Liang S, Gao C. Aligned PLLA nanofibrous scaffolds coated with graphene oxide for promoting neural cell growth. Acta Biomater. 2016; 37: 131-42.

[48] Jia L, Prabhakaran MP, Qin X, Ramakrishna S. Stem cell differentiation on electrospun nanofibrous substrates for vascular tissue engineering. Mater Sci Eng C Mater Biol Appl. 2013; 33: 4640-50.

[49] Ando M, Kawamura H, Kitada H, Sekimoto Y, Inoue T, Tajitsu Y. Pressure-sensitive touch panel based on piezoelectric poly(L-lactic acid) film. Jpn J Appl Phys. 2013; 52: 09KD17.

[50] Curry EJ, Ke K, Chorsi MT, Wrobel KS, Miller AN, 3rd, Patel A, et al. Biodegradable piezoelectric force sensor. Proc Natl Acad Sci USA. 2018; 115: 909-14.

[51] Yang Q, Guo J, Liu Y, Guan F, Sun F, Gong X. Preparation and characterization of poly(3-hydroxybutyrate-co-4-hydroxybutyrate)/gelatin composite nanofibrous. Surfaces and Interfaces. 2022; 33: 102231. https://doi.org/10.1016/j.surfin.2022.102231.

[52] Ribeiro C, Sencadas V, Correia DM, Lanceros-Mendez S. Piezoelectric polymers as biomaterials for tissue engineering applications. Colloids Surf B Biointerfaces. 2015; 136: 46-55.

[53] Genchi GG, Ceseracciu L, Marino A, Labardi M, Marras S, Pignatelli F, et al. P(VDF-TrFE)/BaTiO3 nanoparticle composite films mediate piezoelectric stimulation and promote differentiation of SH-SY5Y Neuroblastoma cells. Adv Healthc Mater. 2016; 5: 1808-20.

[54] Hickey DJ, Ercan B, Sun L, Webster TJ. Adding MgO nanoparticles to hydroxyapatite-PLLA nanocomposites for improved bone tissue engineering applications. Acta Biomater. 2015; 14: 175-84.

[55] Degli Esposti M, Chiellini F, Bondioli F, Morselli D, Fabbri P. Highly porous PHB-based bioactive scaffolds for bone tissue engineering by in situ synthesis of hydroxyapatite. Mater Sci Eng C Mater Biol Appl. 2019; 100: 286-96.

[56] Bunde RL, Jarvi EJ, Rosentreter JJ. Piezoelectric quartz crystal biosensors. Talanta. 1998; 46: 1223-36.

[57] Curie J, Curie P. Development by pressure of polar electricity in hemihedral crystals with inclined faces. Bull Soc Min de France. 1880; 3: 90-3.

[58] Hao J, Li W, Zhai J, Chen H. Progress in high-strain perovskite piezoelectric ceramics. Materials Science and Engineering: R: Reports. 2019; 135: 1-57.

[59] Ozcelik B, Ergun C, Liu H. A study on calcium phosphate/barium titanate composites: phase characterization, piezoelectric property, and cytocompatibility. J Aust Ceram Soc. 2020; 56: 1197-216.

[60] Tan Y, Zhang J, Wu Y, Wang C, Koval V, Shi B, et al. Unfolding grain size effects in barium titanate ferroelectric ceramics. Sci Rep. 2015; 5: 9953.

[61] Baxter FR, Bowen CR, Turner IG, Dent AC. Electrically active bioceramics: a review of interfacial responses. Ann Biomed Eng. 2010; 38: 2079-92.

[62] Tang Y, Wu C, Wu Z, Hu L, Zhang W, Zhao K. Fabrication and in vitro biological properties of piezoelectric bioceramics for bone regeneration. Sci Rep. 2017; 7: 43360.

[63] Ciofani G, Ricotti L, Canale C, ’Alessandro D D, Berrettini S, Mazzolai B, et al. Effects of barium titanate nanoparticles on proliferation and differentiation of rat mesenchymal stem cells. Colloids Surf B Biointerfaces. 2013; 102: 312-20.

[64] Liu L, Chen B, Liu K, Gao J, Ye Y, Wang Z, et al. Wireless manipulation of magnetic/piezoelectric micromotors for precise neural stem-like cell stimulation. Adv Funct Mater. 2020; 30: 1910108.

[65] Xiang Z, Xu L, Shan Y, Cui X, Shi B, Xi Y, et al. Tumor microenviroment-responsive self-assembly of barium titanate nanoparticles with enhanced piezoelectric catalysis capabilities for efficient tumor therapy. Bioact Mater. 2024; 33: 251-61.

[66] Yu S-W, Kuo S-T, Tuan W-H, Tsai Y-Y, Wang S-F. Cytotoxicity and degradation behavior of potassium sodium niobate piezoelectric ceramics. Ceram Int. 2012; 38: 2845-50.

[67] Yao T, Chen J, Wang Z, Zhai J, Li Y, Xing J, et al. The antibacterial effect of potassium-sodium niobate ceramics based on controlling piezoelectric properties. Colloids Surf B Biointerfaces. 2019; 175: 463-8.

[68] Ahamed M, Akhtar MJ, Khan MAM, Alhadlaq HA, Alshamsan A. Barium Titanate (BaTiO(3)) nanoparticles exert cytotoxicity through oxidative stress in human lung carcinoma (A549) cells. Nanomaterials (Basel). 2020; 10: 10.

[69] Busuioc C, Voicu G, Jinga S-I, Mitran V, Cimpean A. The influence of barium titanate on the biological properties of collagen-hydroxiapatite composite scaffolds. Mater Lett. 2019; 253: 317-22.

[70] Polley C, Distler T, Detsch R, Lund H, Springer A, Boccaccini AR, et al. 3D printing of piezoelectric barium Titanate-hydroxyapatite scaffolds with interconnected porosity for bone tissue engineering. Materials (Basel). 2020; 13: 1773.

[71] Ferrone E, Araneo R, Notargiacomo A, Pea M, Rinaldi A. ZnO nanostructures and electrospun ZnO-polymeric hybrid nanomaterials in biomedical, health, and sustainability applications. Nanomaterials (Basel). 2019; 9: 1449.

[72] Anandhan SV, Krishnan UM. Boron nitride nanotube scaffolds: emergence of a new era in regenerative medicine. Biomed Mater. 2021; 16: 044105. https://doi.org/10.1088/1748-605X/abf27d.

[73] Verma AS, Kumar D, Dubey AK. A review of an innovative concept to increase the toughness of the ceramics by piezoelectric secondary phases. Ceram Int. 2018; 44: 16119-27.

[74] Verma AS, Sharma A, Kumar A, Mukhopadhyay A, Kumar D, Dubey AK. Multifunctional response of piezoelectric sodium potassium Niobate (NKN)-toughened hydroxyapatite-based biocomposites. ACS Applied Bio Materials. 2020; 3: 5287-99.

[75] Kang Z, Yan X, Zhao L, Liao Q, Zhao K, Du H, et al. Gold nanoparticle/ZnO nanorod hybrids for enhanced reactive oxygen species generation and photodynamic therapy. Nano Res. 2015; 8: 2004-14.

[76] Zhang Y, An Q, Zhang S, Ma Z, Hu X, Feng M, et al. A healing promoting wound dressing with tailor-made antibacterial potency employing piezocatalytic processes in multi-functional nanocomposites. Nanoscale. 2022; 14: 2649-59.

[77] Panda AKKR, Gebrekrstos A, Bose S, Markandeya YS, Mehta B, et al. Tunable substrate functionalities direct stem cell fate toward Electrophysiologically distinguishable neuron-like and glial-like cells. ACS Appl Mater Interfaces. 2021; 13: 164-85.

[78] Le AT, Ahmadipour M, Pung S-Y. A review on ZnO-based piezoelectric nanogenerators: synthesis, characterization techniques, performance enhancement and applications. J Alloys Compd. 2020; 844: 156172. https://doi.org/10.1016/j.jallcom.2020.156172.

[79] Azimi B, Milazzo M, Lazzeri A, Berrettini S, Uddin MJ, Qin Z, et al. Electrospinning piezoelectric Fibers for biocompatible devices. Adv Healthc Mater. 2020; 9: e1901287. https://doi.org/10.1002/adhm.201901287.

[80] Zhang X, Cui X, Wang D, Wang S, Liu Z, Zhao G, et al. Piezoelectric Nanotopography induced neuron-like differentiation of stem cells. Adv Funct Mater. 2019; 29: 1900372.

[81] Gong S, Zhang B, Zhang J, Wang ZL, Ren K. Biocompatible poly(lactic acid)-based hybrid piezoelectric and electret Nanogenerator for electronic skin applications. Adv Funct Mater. 2020; 30: 1908724.

[82] Neuss S, Apel C, Buttler P, Denecke B, Dhanasingh A, Ding X, et al. Assessment of stem cell/biomaterial combinations for stem cell-based tissue engineering. Biomaterials. 2008; 29: 302-13.

[83] Hoop M, Chen XZ, Ferrari A, Mushtaq F, Ghazaryan G, Tervoort T, et al. Ultrasound-mediated piezoelectric differentiation of neuron-like PC12 cells on PVDF membranes. Sci Rep. 2017; 7: 4028.

[84] Lins LC, Wianny F, Livi S, Dehay C, Duchet-Rumeau J, Gerard JF. Effect of polyvinylidene fluoride electrospun fiber orientation on neural stem cell differentiation. J Biomed Mater Res B Appl Biomater. 2017; 105: 2376-93.

[85] Lv J, Cheng Y. Fluoropolymers in biomedical applications: state-of-the-art and future perspectives. Chem Soc Rev. 2021; 50: 5435-67.

[86] Fu Q, Liu Y, Liu T, Mo J, Zhang W, Zhang S, et al. Air-permeable cellulosic triboelectric materials for self-powered healthcare products. Nano Energy. 2022; 102: 107739. https://doi.org/10.1016/j.nanoen.2022.107739.

[87] Lu L, Yang B, Zhai Y, Liu J. Electrospinning core-sheath piezoelectric microfibers for self-powered stitchable sensor. Nano Energy. 2020; 76: 104966. https://doi.org/10.1016/j.nanoen.2020.104966.

[88] Chelakara Satyanarayana K, Bolton K. Molecular dynamics simulations of α-to β-poly(vinylidene fluoride) phase change by stretching and poling. Polymer. 2012; 53: 2927-34.

[89] Weber N, Lee YS, Shanmugasundaram S, Jaffe M, Arinzeh TL. Characterization and in vitro cytocompatibility of piezoelectric electrospun scaffolds. Acta Biomater. 2010; 6: 3550- 6.

[90] Tandon B, Blaker JJ, Cartmell SH. Piezoelectric materials as stimulatory biomedical materials and scaffolds for bone repair. Acta Biomater. 2018; 73: 1-20.

[91] Sun F-C, Dongare AM, Asandei AD, Pamir Alpay S, Nakhmanson S. Temperature dependent structural, elastic, and polar properties of ferroelectric polyvinylidene fluoride (PVDF) and trifluoroethylene (TrFE) copolymers. J Mater Chem C. 2015; 3: 8389-96.

[92] Wang A, Hu M, Zhou L, Qiang X. Self-powered well-aligned P(VDF-TrFE) piezoelectric nanofiber Nanogenerator for modulating an exact electrical stimulation and enhancing the proliferation of Preosteoblasts. Nanomaterials (Basel). 2019; 9: 349.

[93] Meng N, Zhu X, Mao R, Reece MJ, Bilotti E. Nanoscale interfacial electroactivity in PVDF/PVDF-TrFE blended films with enhanced dielectric and ferroelectric properties. J Mater Chem C. 2017; 5: 3296-305.

[94] Casalini T, Rossi F, Castrovinci A, Perale G. A perspective on Polylactic acid-based polymers use for nanoparticles synthesis and applications. Front Bioeng Biotechnol. 2019; 7: 259.

[95] Maleki H, Azimi B, Ismaeilimoghadam S, Danti S. Poly(lactic acid)-based electrospun fibrous structures for biomedical applications. Appl Sci. 2022; 12: 3192.

[96] Capuana E, Lopresti F, Ceraulo M, La Carrubba V. Poly-l-lactic acid (PLLA)-based biomaterials for regenerative medicine: a review on processing and applications. Polymers (Basel). 2022; 14: 1153.

[97] Tai Y, Yang S, Yu S, Banerjee A, Myung NV, Nam J. Modulation of piezoelectric properties in electrospun PLLA nanofibers for application-specific self-powered stem cell culture platforms. Nano Energy. 2021; 89: 106444. https://doi.org/10.1016/j.nanoen.2021.106444.

[98] Laycock B, Halley P, Pratt S, Werker A, Lant P. The chemomechanical properties of microbial polyhydroxyalkanoates. Prog Polym Sci. 2014; 39: 397-442.

[99] Paula ACC, Carvalho PH, Martins TMM, Boeloni JN, Cunha PS, Novikoff S, et al. Improved vascularisation but inefficient in vivo bone regeneration of adipose stem cells and poly-3-hydroxybutyrate-co-3-hydroxyvalerate scaffolds in xeno-free conditions. Mater Sci Eng C. 2020; 107: 110301. https://doi.org/10.1016/j.msec.2019.110301.

[100] Li M, Jie Y, Shao L-H, Guo Y, Cao X, Wang N, et al. All-in-one cellulose based hybrid tribo/piezoelectric nanogenerator. Nano Res. 2019; 12: 1831-5.

[101] Sun J, Guo H, Ribera J, Wu C, Tu K, Binelli M, et al. Sustainable and biodegradable wood sponge piezoelectric Nanogenerator for sensing and energy harvesting applications. ACS Nano. 2020; 14: 14665-74.

[102] Hanninen A, Sarlin E, Lyyra I, Salpavaara T, Kellomaki M, Tuukkanen S. Nanocellulose and chitosan based films as low cost, green piezoelectric materials. Carbohydr Polym. 2018; 202: 418-24.

[103] Wang L, Cheng T, Lian W, Zhang M, Lu B, Dong B, et al. Flexible layered cotton cellulose-based nanofibrous membranes for piezoelectric energy harvesting and self-powered sensing. Carbohydr Polym. 2022; 275: 118740. https://doi.org/10.1016/j.carbpol.2021.118740.

[104] Zong Y, Wang R, Xu S, Zhang R, Zhang Z. Flexible piezoelectric Nanogenerator based on cellulose Nanofibril/MXene composite aerogels for Low-frequency energy harvesting. ACS Applied Nano Materials. 2023; 6: 9021-31.

[105] Song Y, Shi Z, Hu G-H, Xiong C, Isogai A, Yang Q. Recent advances in cellulose-based piezoelectric and triboelectric nanogenerators for energy harvesting: a review. J Mater Chem A. 2021; 9: 1910-37.

[106] de Marzo G, Mastronardi VM, Algieri L, Vergari F, Pisano F, Fachechi L, et al. Sustainable, flexible, and biocompatible enhanced piezoelectric chitosan thin film for compliant Piezosensors for human health. Advanced Electronic Materials. 2022; 9: 2200069.

[107] Praveen E, Murugan S, Jayakumar K. Investigations on the existence of piezoelectric property of a bio-polymer-chitosan and its application in vibration sensors. RSC Adv. 2017; 7: 35490-5.

[108] Wang R, Sui J, Wang X. Natural piezoelectric biomaterials: a biocompatible and sustainable building block for biomedical devices. ACS Nano. 2022; 16: 17708-28.

[109] Vasileva D, Vasilev S, Kholkin AL, Shur VY. Domain diversity and polarization switching in amino acid beta-glycine. Materials (Basel). 2019; 12: 1223. https://doi.org/10.3390/ma12081223.

[110] Rodríguez JS, Costa G, da Silva MB, Silva BP, Honório LJ, de Lima-Neto P, et al. Structural and optoelectronic properties of the α-, β-, and γ-glycine polymorphs and the glycine Dihydrate crystal: a DFT study. Cryst Growth Des. 2019; 19: 5204-17.

[111] Hosseini ES, Manjakkal L, Shakthivel D, Dahiya R. Glycine-chitosan-based flexible biodegradable piezoelectric pressure sensor. ACS Appl Mater Interfaces. 2020; 12: 9008-16.

[112] Ukasi S, Jutapukti P, Ninthub C, Pinpru N, Pakawanit P, Vittayakorn W, et al. Gamma glycine enhances efficiency of organic hybrid piezoelectric-triboelectric nanogenerators. Nano Energy. 2024; 119: 109045.

[113] Noisak J, Charoonsuk T, Pongampai S, Pinpru N, Pakawanit P, Vittayakorn W, et al. Towards the preparation of organic ferroelectric composites: fabrication of a gamma-glycine-bacterial cellulose composite via cold sintering process. Journal of Materials Research and Technology. 2023; 25: 4749-60.

[114] Guerin S, Tofail SAM, Thompson D. Longitudinal piezoelectricity in orthorhombic amino acid crystal films. Cryst Growth Des. 2018; 18: 4844-8.

[115] Guerin S, O’Donnell J, Haq EU, McKeown C, Silien C, Rhen FMF, et al. Racemic amino acid piezoelectric transducer. Phys Rev Lett. 2019; 122: 047701.

[116] Caetano EWS, Silva JB, Bruno CHV, Albuquerque EL, Esilva BP, Dos Santos RCR, et al. Investigating the molecular crystals of L-alanine, DL-alanine, β-alanine, and alanine hydrogen chloride: experimental and DFT analysis of structural and optoelectronic properties. J Mol Struct. 2024; 1300: 137228.

[117] O’Donnell J, Sarkar SM, Guerin S, Borda GG, Silien C, Soulimane T, et al. Piezoelectricity in the proteinogenic amino acid L-leucine: a novel piezoactive bioelectret. IEEE Trans Dielectr Electr Insul. 2020; 27: 1465-8.

[118] Ji W, Xue B, Arnon ZA, Yuan H, Bera S, Li Q, et al. Rigid tightly packed amino acid crystals as functional supramolecular materials. ACS Nano. 2019; 13: 14477-85.

[119] Cheng Y, Xu J, Li L, Cai P, Li Y, Jiang Q, et al. Boosting the piezoelectric sensitivity of amino acid crystals by mechanical annealing for the engineering of fully degradable force sensors. Adv Sci (Weinh). 2023; 10: e2207269. https://doi.org/10.1002/advs.202207269.

[120] Tao K, Hu W, Xue B, Chovan D, Brown N, Shimon LJW, et al. Bioinspired stable and Photoluminescent assemblies for power generation. Adv Mater. 2019; 31: e1807481. https://doi.org/10.1002/adma.201807481.

[121] Yang J, Chen M, Lee H, Xu Z, Zhou Z, Feng SP, et al. Three-dimensional printing of self-assembled dipeptides. ACS Appl Mater Interfaces. 2021; 13: 20573-80.

[122] Kim D, Han SA, Kim JH, Lee JH, Kim SW, Lee SW. Biomolecular piezoelectric materials: from amino acids to living tissues. Adv Mater. 2020; 32: e1906989. https://doi.org/10.1002/adma.201906989.

[123] Vivekananthan V, Alluri NR, Purusothaman Y, Chandrasekhar A, Selvarajan S, Kim SJ. Biocompatible collagen Nanofibrils: An approach for sustainable energy harvesting and battery-free humidity sensor applications. ACS Appl Mater Interfaces. 2018; 10: 18650-6.

[124] Sencadas V, Garvey C, Mudie S, Kirkensgaard JJK, Gouadec G, Hauser S. Electroactive properties of electrospun silk fibroin for energy harvesting applications. Nano Energy. 2019; 66: 104106.

[125] Niu Q, Wei H, Hsiao BS, Zhang Y. Biodegradable silk fibroin-based bio-piezoelectric/triboelectric nanogenerators as self-powered electronic devices. Nano Energy. 2022; 96: 107101.

[126] Liu J-H, Li W-D, Jia J, Tang C-Y, Wang S, Yu P, et al. Structure-regenerated silk fibroin with boosted piezoelectricity for disposable and biodegradable oral healthcare device. Nano Energy. 2022; 103: 107787.

[127] Sohn C, Kim H, Han J, Lee K-T, Šutka A, Jeong CK. Generating electricity from molecular bonding-correlated piezoresonse of biodegradable silk nanofibers. Nano Energy. 2022; 103: 107844.

[128] Zhang Y, Li J, Boutis GS. The coupled bio-chemo-electro-mechanical behavior of glucose exposed arterial elastin. J Phys D Appl Phys. 2017; 50: 50.

[129] Jiang P, Yan F, Nasr Esfahani E, Xie S, Zou D, Liu X, et al. Electromechanical coupling of murine lung tissues probed by Piezoresponse force microscopy. ACS Biomater Sci Eng. 2017; 3: 1827-35.

[130] Yan J, Liu M, Jeong YG, Kang W, Li L, Zhao Y, et al. Performance enhancements in poly(vinylidene fluoride)-based piezoelectric nanogenerators for efficient energy harvesting. Nano Energy. 2019; 56: 662-92.

[131] Jin C, Hao N, Xu Z, Trase I, Nie Y, Dong L, et al. Flexible piezoelectric Nanogenerators using metal-doped ZnO-PVDF films. Sens Actuators A Phys. 2020; 305: 111912. https://doi.org/10.1016/j.sna.2020.111912.

[132] Panda AK, Sitaramgupta VSNT, Pandya HJ, Basu B. Electrical stimulation waveform-dependent osteogenesis on PVDF/BaTiO3 composite using a customized and programmable cell stimulator. Biotechnol Bioeng. 2022; 119: 1578-97.

[133] Chanmal CV, Jog JP. Electrospun PVDF/BaTiO3 nanocomposites: polymorphism and thermal emissivity studies. Int J Plast Technol. 2011; 15: 1-9.

[134] Hou Y, Deng Y, Wang Y, Gao H. Uniform distribution of low content BaTiO3 nanoparticles in poly(vinylidene fluoride) nanocomposite: toward high dielectric breakdown strength and energy storage density. RSC Adv. 2015; 5: 72090-8.

[135] Li J, Zhao C, Xia K, Liu X, Li D, Han J. Enhanced piezoelectric output of the PVDF-TrFE/ZnO flexible piezoelectric nanogenerator by surface modification. Appl Surf Sci. 2019; 463: 626-34.

[136] Ilyas RA, Zuhri MYM, Norrrahim MNF, Misenan MSM, Jenol MA, Samsudin SA, et al. Natural Fiber-reinforced Polycaprolactone green and hybrid biocomposites for various advanced applications. Polymers (Basel). 2022; 14: 182.

[137] Hwang TI, Kim JI, Joshi MK, Park CH, Kim CS. Simultaneous regeneration of calcium lactate and cellulose into PCL nanofiber for biomedical application. Carbohydr Polym. 2019; 212: 21-9.

[138] Woodruff MA, Hutmacher DW. The return of a forgotten polymer-Polycaprolactone in the 21st century. Prog Polym Sci. 2010; 35: 1217-56.

[139] Dwivedi R, Kumar S, Pandey R, Mahajan A, Nandana D, Katti DS, et al. Polycaprolactone as biomaterial for bone scaffolds: review of literature. J Oral Biol Craniofac Res. 2020; 10: 381-8.

[140] Liu J, Gu H, Liu Q, Ren L, Li G. An intelligent material for tissue reconstruction: the piezoelectric property of polycaprolactone/barium titanate composites. Mater Lett. 2019; 236: 686-9.

[141] Farokhi M, Mottaghitalab F, Saeb MR, Shojaei S, Zarrin NK, Thomas S, et al. Conductive biomaterials as substrates for neural stem cells differentiation towards neuronal lineage cells. Macromol Biosci. 2021; 21: e2000123. https://doi.org/10.1002/mabi.202000123.

[142] Khorshidi S, Karkhaneh A. Hydrogel/fiber conductive scaffold for bone tissue engineering. J Biomed Mater Res A. 2018; 106: 718-24.

[143] Shin SR, Aghaei-Ghareh-Bolagh B, Dang TT, Topkaya SN, Gao X, Yang SY, et al. Cell-laden microengineered and mechanically tunable hybrid hydrogels of gelatin and graphene oxide. Adv Mater. 2013; 25: 6385-91.

[144] Li J, Liu X, Crook JM, Wallace GG. Electrical stimulation-induced osteogenesis of human adipose derived stem cells using a conductive graphene-cellulose scaffold. Mater Sci Eng C Mater Biol Appl. 2020; 107: 110312. https://doi.org/10.1016/j.msec.2019.110312.

[145] Agarwal G, Kumar N, Srivastava A. Highly elastic, electro-conductive, immunomodulatory graphene crosslinked collagen cryogel for spinal cord regeneration. Mater Sci Eng C Mater Biol Appl. 2021; 118: 111518. https://doi.org/10.1016/j.msec.2020.111518.

[146] Berger C, Song Z, Li X, Wu X, Brown N, Naud C, et al. Electronic confinement and coherence in patterned epitaxial graphene. Science. 2006; 312: 1191-6.

[147] Nizami MZI, Takashiba S, Nishina Y. Graphene oxide: a new direction in dentistry. Appl Mater Today. 2020; 19: 100576. https://doi.org/10.1016/j.apmt.2020.100576.

[148] Liu S, Zhou C, Mou S, Li J, Zhou M, Zeng Y, et al. Biocompatible graphene oxide-collagen composite aerogel for enhanced stiffness and in situ bone regeneration. Mater Sci Eng C Mater Biol Appl. 2019; 105: 110137. https://doi.org/10.1016/j.msec.2019.110137.

[149] Eivazzadeh-Keihan R, Maleki A, de la Guardia M, Bani MS, Chenab KK, Pashazadeh-Panahi P, et al. Carbon based nanomaterials for tissue engineering of bone: building new bone on small black scaffolds: a review. J Adv Res. 2019; 18: 185-201.

[150] Qian Y, Song J, Zhao X, Chen W, Ouyang Y, Yuan W, et al. 3D fabrication with integration Molding of a graphene oxide/Polycaprolactone Nanoscaffold for neurite regeneration and angiogenesis. Adv Sci (Weinh). 2018; 5: 1700499.

[151] Xie H, Cao T, Rodriguez-Lozano FJ, Luong-Van EK, Rosa V. Graphene for the development of the next-generation of biocomposites for dental and medical applications. Dent Mater. 2017; 33: 765-74.

[152] Yadid M, Feiner R, Dvir T. Gold nanoparticle-integrated scaffolds for tissue engineering and regenerative medicine. Nano Lett. 2019; 19: 2198-206.

[153] Fathi-Achachelouei M, Knopf-Marques H, Ribeiro da Silva CE, Barthes J, Bat E, Tezcaner A, et al. Use of nanoparticles in tissue engineering and regenerative medicine. Front Bioeng Biotechnol. 2019; 7: 113.

[154] Shevach M, Maoz BM, Feiner R, Shapira A, Dvir T. Nanoengineering gold particle composite fibers for cardiac tissue engineering. J Mater Chem B. 2013; 1: 5210-7.

[155] Damle A, Sundaresan R, Rajwade JM, Srivastava P, Naik A. A concise review on implications of silver nanoparticles in bone tissue engineering. Biomater Adv. 2022; 141: 213099. https://doi.org/10.1016/j.bioadv.2022.213099.

[156] Marsich E, Bellomo F, Turco G, Travan A, Donati I, Paoletti S. Nano-composite scaffolds for bone tissue engineering containing silver nanoparticles: preparation, characterization and biological properties. J Mater Sci Mater Med. 2013; 24: 1799-807.

[157] Campoccia D, Montanaro L, Arciola CR. A review of the clinical implications of anti-infective biomaterials and infection-resistant surfaces. Biomaterials. 2013; 34: 8018-29.

[158] Kargozar S, Mozafari M, Ghodrat S, Fiume E, Baino F. Copper-containing bioactive glasses and glass-ceramics: from tissue regeneration to cancer therapeutic strategies. Mater Sci Eng C Mater Biol Appl. 2021; 121: 111741. https://doi.org/10.1016/j.msec.2020.111741.

[159] Janarthanan G, Noh I. Recent trends in metal ion based hydrogel biomaterials for tissue engineering and other biomedical applications. Journal of Materials Science & Technology. 2021; 63: 35-53.

[160] Marin E. Forged to heal: the role of metallic cellular solids in bone tissue engineering. Mater Today Bio. 2023; 23: 100777. https://doi.org/10.1016/j.mtbio.2023.100777.

[161] Adhikari U, An X, Rijal N, Hopkins T, Khanal S, Chavez T, et al. Embedding magnesium metallic particles in polycaprolactone nanofiber mesh improves applicability for biomedical applications. Acta Biomater. 2019; 98: 215-34.

[162] Petre DG, Leeuwenburgh SCG. The use of Fibers in bone tissue engineering. Tissue Eng Part B Rev. 2022; 28: 141-59.

[163] Jiang S, Sun Y, Cui X, Huang X, He Y, Ji S, et al. Enhanced drug loading capacity of polypyrrole nanowire network for controlled drug release. Synth Met. 2013; 163: 19-23.

[164] Zhou L, Fan L, Yi X, Zhou Z, Liu C, Fu R, et al. Soft conducting polymer hydrogels cross-linked and doped by tannic acid for spinal cord injury repair. ACS Nano. 2018; 12: 10957-67.

[165] Deng P, Chen F, Zhang H, Chen Y, Zhou J. Multifunctional double-layer composite hydrogel conduit based on chitosan for peripheral nerve repairing. Adv Healthc Mater. 2022; 11:e2200115. https://doi.org/10.1002/adhm.202200115.

[166] Guarino V, Alvarez-Perez MA, Borriello A, Napolitano T, Ambrosio L. Conductive PANi/PEGDA macroporous hydrogels for nerve regeneration. Adv Healthc Mater. 2013; 2: 218-27.

[167] Talikowska M, Fu X, Lisak G. Application of conducting polymers to wound care and skin tissue engineering: a review. Biosens Bioelectron. 2019; 135: 50-63.

[168] Olvera D, Monaghan MG. Electroactive material-based biosensors for detection and drug delivery. Adv Drug Deliv Rev. 2021; 170: 396-424.

[169] Bhattarai DP, Tiwari AP, Maharjan B, Tumurbaatar B, Park CH, Kim CS. Sacrificial template-based synthetic approach of polypyrrole hollow fibers for photothermal therapy. J Colloid Interface Sci. 2019; 534: 447-58.

[170] Liang Y, Goh JC. Polypyrrole-incorporated conducting constructs for tissue engineering applications: a review. Bioelectricity. 2020; 2: 101-19.

[171] Zhao Y, Liang Y, Ding S, Zhang K, Mao HQ, Yang Y. Application of conductive PPy/SF composite scaffold and electrical stimulation for neural tissue engineering. Biomaterials. 2020; 255: 120164. https://doi.org/10.1016/j.biomaterials.2020.120164.

[172] Ghasemi-Mobarakeh L, Prabhakaran MP, Morshed M, Nasr-Esfahani MH, Baharvand H, Kiani S, et al. Application of conductive polymers, scaffolds and electrical stimulation for nerve tissue engineering. J Tissue Eng Regen Med. 2011; 5: e17-35.

[173] Naureen B, Haseeb A, Basirun WJ, Muhamad F. Recent advances in tissue engineering scaffolds based on polyurethane and modified polyurethane. Mater Sci Eng C Mater Biol Appl. 2021; 118: 111228.

[174] Luculescu CR, Acasandrei AM, Mustaciosu CC, Zamfirescu M, Dinescu M, Calin BS, et al. Electrically responsive microstructured polypyrrole-polyurethane composites for stimulated osteogenesis. Appl Surf Sci. 2018; 433: 166-76.

[175] Maharjan B, Kaliannagounder VK, Jang SR, Awasthi GP, Bhattarai DP, Choukrani G, et al. In-situ polymerized polypyrrole nanoparticles immobilized poly(epsilon-caprolactone) electrospun conductive scaffolds for bone tissue engineering. Mater Sci Eng C Mater Biol Appl. 2020; 114: 111056.

[176] Li M, Guo Y, Wei Y, MacDiarmid AG, Lelkes PI. Electrospinning polyaniline-contained gelatin nanofibers for tissue engineering applications. Biomaterials. 2006; 27: 2705-15.

[177] Zhao X, Li P, Guo B, Ma PX. Antibacterial and conductive injectable hydrogels based on quaternized chitosan-graft-polyaniline/oxidized dextran for tissue engineering. Acta Biomater. 2015; 26: 236-48.

[178] Liu, Y., Zhang, X., Cao, C., Zhang, Y., Wei, J., Li, Y. j., Liang W., Hu Z., Zhang J., Wei Y., Deng X. Built-in electric fields dramatically induce enhancement of Osseointegration. Adv Funct Mater 2017; 27: 1703771.

[179] Helaehil JV, Helaehil LV, Alves LF, Huang B, Santamaria-Jr M, Bartolo P, et al. Electrical stimulation therapy and HA/TCP composite scaffolds modulate the Wnt pathways in bone regeneration of critical-sized defects. Bioengineering (Basel). 2023; 10: 75.

[180] Leal J, Jedrusik N, Shaner S, Boehler C, Asplund M. SIROF stabilized PEDOT/PSS allows biocompatible and reversible direct current stimulation capable of driving electrotaxis in cells. Biomaterials. 2021; 275: 120949. https://doi.org/10.1016/j.biomaterials.2021.120949.

[181] Sharma A, Panwar V, Mondal B, Prasher D, Bera MK, Thomas J, et al. Electrical stimulation induced by a piezo-driven triboelectric nanogenerator and electroactive hydrogel composite, accelerate wound repair. Nano Energy. 2022; 99: 107419.

[182] Wu P, Shen L, Liu HF, Zou XH, Zhao J, Huang Y, et al. The marriage of immunomodulatory, angiogenic, and osteogenic capabilities in a piezoelectric hydrogel tissue engineering scaffold for military medicine. Mil Med Res. 2023; 10: 35.

[183] ’Alessandro D D, Ricci C, Milazzo M, Strangis G, Forli F, Buda G, et al. Piezoelectric signals in vascularized bone regeneration. Biomol Ther. 2021; 11: 1731.

[184] Liu W, Li X, Jiao Y, Wu C, Guo S, Xiao X, et al. Biological effects of a three-dimensionally printed Ti6Al4V scaffold coated with piezoelectric BaTiO(3) nanoparticles on bone formation. ACS Appl Mater Interfaces. 2020; 12: 51885-903.

[185] Yang C, Ji J, Lv Y, Li Z, Luo D. Application of piezoelectric material and devices in bone regeneration. Nanomaterials (Basel). 2022; 12: 4386.

[186] Ribeiro C, Parssinen J, Sencadas V, Correia V, Miettinen S, Hytonen VP, et al. Dynamic piezoelectric stimulation enhances osteogenic differentiation of human adipose stem cells. J Biomed Mater Res A. 2015; 103: 2172-5.

[187] Kitsara M, Blanquer A, Murillo G, Humblot V, De Braganca Vieira S, Nogues C, et al. Permanently hydrophilic, piezoelectric PVDF nanofibrous scaffolds promoting unaided electromechanical stimulation on osteoblasts. Nanoscale. 2019; 11: 8906-17.

[188] Saburi E, Islami M, Hosseinzadeh S, Moghadam AS, Mansour RN, Azadian E, et al. In vitro osteogenic differentiation potential of the human induced pluripotent stem cells augments when grown on graphene oxide-modified nanofibers. Gene. 2019; 696: 72-9.

[189] Shuai C, Zeng Z, Yang Y, Qi F, Peng S, Yang W, et al. Graphene oxide assists polyvinylidene fluoride scaffold to reconstruct electrical microenvironment of bone tissue. Mater Des. 2020; 190: 108564. https://doi.org/10.1016/j.matdes.2020.108564.

[190] Genchi GG, Sinibaldi E, Ceseracciu L, Labardi M, Marino A, Marras S, et al. Ultrasound-activated piezoelectric P(VDF-TrFE)/boron nitride nanotube composite films promote differentiation of human SaOS-2 osteoblast-like cells. Nanomedicine. 2018; 14: 2421-32.

[191] Pereira JD, Camargo RC, Filho JC, Alves N, Rodriguez-Perez MA, Constantino CJ. Biomaterials from blends of fluoropolymers and corn starch-implant and structural aspects. Mater Sci Eng C Mater Biol Appl. 2014; 36: 226-36.

[192] Gupte MJ, Swanson WB, Hu J, Jin X, Ma H, Zhang Z, et al. Pore size directs bone marrow stromal cell fate and tissue regeneration in nanofibrous macroporous scaffolds by mediating vascularization. Acta Biomater. 2018; 82: 1-11.

[193] Lai Y-H, Chen Y-H, Pal A, Chou S-H, Chang S-J, Huang EW, et al. Regulation of cell differentiation via synergistic self-powered stimulation and degradation behavior of a biodegradable composite piezoelectric scaffold for cartilage tissue. Nano Energy. 2021; 90: 106545. https://doi.org/10.1016/j.nanoen.2021.106545.

[194] de Siqueira L, Ribeiro N, Paredes MBA, Grenho L, Cunha-Reis C, Triches ES, et al. Influence of PLLA/PCL/HA scaffold Fiber orientation on mechanical properties and osteoblast behavior. Materials (Basel). 2019; 12: 3879.

[195] Pan Z, Ding J. Poly(lactide-co-glycolide) porous scaffolds for tissue engineering and regenerative medicine. Interface Focus. 2012; 2: 366-77.

[196] Babilotte J, Martin B, Guduric V, Bareille R, Agniel R, Roques S, et al. Development and characterization of a PLGA-HA composite material to fabricate 3D-printed scaffolds for bone tissue engineering. Mater Sci Eng C Mater Biol Appl. 2021; 118: 111334. https://doi.org/10.1016/j.msec.2020.111334.

[197] Fazeli N, Arefian E, Irani S, Ardeshirylajimi A, Seyedjafari E. 3D-printed PCL scaffolds coated with Nanobioceramics enhance osteogenic differentiation of stem cells. ACS Omega. 2021; 6: 35284-96.

[198] Baino F, Fiorilli S, Vitale-Brovarone C. Bioactive glass-based materials with hierarchical porosity for medical applications: review of recent advances. Acta Biomater. 2016; 42: 18-32.

[199] Daris B, Knez Z. Poly(3-hydroxybutyrate): promising biomaterial for bone tissue engineering. Acta Pharma. 2020; 70: 1-15.

[200] Volkov AV, Muraev AA, Zharkova II, Voinova VV, Akoulina EA, Zhuikov VA, et al. Poly(3-hydroxybutyrate)/hydroxyapatite/alginate scaffolds seeded with mesenchymal stem cells enhance the regeneration of critical-sized bone defect. Mater Sci Eng C Mater Biol Appl. 2020; 114: 110991. https://doi.org/10.1016/j.msec.2020.110991.

[201] Mohan A, Girdhar M, Kumar R, Chaturvedi HS, Vadhel A, Solanki PR, et al. Polyhydroxybutyrate-based nanocomposites for bone tissue engineering. Pharmaceuticals (Basel). 2021; 14: 1163.

[202] Mirzaei A, Saburi E, Enderami SE, Barati Bagherabad M, Enderami SE, Chokami M, et al. Synergistic effects of polyaniline and pulsed electromagnetic field to stem cells osteogenic differentiation on polyvinylidene fluoride scaffold. Artif Cells Nanomed Biotechnol. 2019; 47: 3058-66.

[203] Chernozem RV, Guselnikova O, Surmeneva MA, Postnikov PS, Abalymov AA, Parakhonskiy BV, et al. Diazonium chemistry surface treatment of piezoelectric polyhydroxybutyrate scaffolds for enhanced osteoblastic cell growth. Appl Mater Today. 2020; 20: 100758. https://doi.org/10.1016/j.apmt.2020.100758.

[204] Eftekhari BS, Eskandari M, Janmey PA, Samadikuchaksaraei A, Gholipourmalekabadi M.Surface topography and electrical Signaling: single and synergistic effects on neural differentiation of stem cells. Adv Funct Mater. 2020; 30: 1907792.

[205] Yang Y, Yin X, Wang H, Qiu W, Li L, Li F, et al. Engineering a wirelessly self-powered and electroconductive scaffold to promote peripheral nerve regeneration. Nano Energy. 2023; 107: 108145. https://doi.org/10.1016/j.nanoen.2022.108145.

[206] Lee Y-S, Livingston Arinzeh T. Electrospun Nanofibrous materials for neural tissue engineering. Polymers. 2011; 3: 413-26.

[207] Jun I, Han HS, Edwards JR, Jeon H. Electrospun fibrous scaffolds for tissue engineering: viewpoints on architecture and fabrication. Int J Mol Sci. 2018; 19: 745.

[208] Wang J, Cheng Y, Chen L, Zhu T, Ye K, Jia C, et al. In vitro and in vivo studies of electroactive reduced graphene oxide-modified nanofiber scaffolds for peripheral nerve regeneration. Acta Biomater. 2019; 84: 98-113.

[209] Abzan N, Kharaziha M, Labbaf S. Development of three-dimensional piezoelectric polyvinylidene fluoride-graphene oxide scaffold by non-solvent induced phase separation method for nerve tissue engineering. Mater Des. 2019; 167: 107636. https://doi.org/10.1016/j.matdes.2019.107636.

[210] Cheng Y, Xu Y, Qian Y, Chen X, Ouyang Y, Yuan W-E. 3D structured self-powered PVDF/PCL scaffolds for peripheral nerve regeneration. Nano Energy. 2020; 69: 104411. https://doi.org/10.1016/j.nanoen.2019.104411.

[211] Balint R, Cassidy NJ, Cartmell SH. Conductive polymers: towards a smart biomaterial for tissue engineering. Acta Biomater. 2014; 10: 2341-53.

[212] Zou Y, Qin J, Huang Z, Yin G, Pu X, He D. Fabrication of aligned conducting PPy-PLLA Fiber films and their electrically controlled guidance and orientation for neurites. ACS Appl Mater Interfaces. 2016; 8: 12576-82.

[213] Zhou X, Yang A, Huang Z, Yin G, Pu X, Jin J. Enhancement of neurite adhesion, alignment and elongation on conductive polypyrrole-poly(lactide acid) fibers with cell-derived extracellular matrix. Colloids Surf B Biointerfaces. 2017; 149: 217-25.

[214] Chen X, Liu C, Huang Z, Pu X, Shang L, Yin G, et al. Preparation of carboxylic graphene oxide-composited polypyrrole conduits and their effect on sciatic nerve repair under electrical stimulation. J Biomed Mater Res A. 2019; 107: 2784-95.

[215] Shang L, Huang Z, Pu X, Yin G, Chen X. Preparation of graphene oxide-doped Polypyrrole composite films with stable conductivity and their effect on the elongation and alignment of neurite. ACS Biomater Sci Eng. 2019; 5: 1268-78.

[216] Prabhakaran MP, Ghasemi-Mobarakeh L, Jin G, Ramakrishna S. Electrospun conducting polymer nanofibers and electrical stimulation of nerve stem cells. J Biosci Bioeng. 2011; 112: 501-7.

[217] Kao FC, Ho HH, Chiu PY, Hsieh MK, Liao JC, Lai PL, et al. Self-assisted wound healing using piezoelectric and triboelectric nanogenerators. Sci Technol Adv Mater. 2022; 23: 1-16.

[218] Tai G, Tai M, Zhao M. Electrically stimulated cell migration and its contribution to wound healing. Burns Trauma. 2018; 6: 20.

[219] Goonoo N, Gimie F, Ait-Arsa I, Cordonin C, Andries J, Jhurry D, et al. Piezoelectric core-shell PHBV/PDX blend scaffolds for reduced superficial wound contraction and scarless tissue regeneration. Biomater Sci. 2021; 9: 5259-74.

[220] Chen Y, Ye M, Song L, Zhang J, Yang Y, Luo S, et al. Piezoelectric and photothermal dual functional film for enhanced dermal wound regeneration via upregulation of Hsp90 and HIF-1α. Appl Mater Today. 2020; 20: 100756. https://doi.org/10.1016/j.apmt.2020.100756.

[221] Liang Y, Zhao X, Hu T, Chen B, Yin Z, Ma PX, et al. Adhesive Hemostatic conducting injectable composite hydrogels with sustained drug release and Photothermal antibacterial activity to promote full-thickness skin regeneration during wound healing. Small. 2019; 15: e1900046. https://doi.org/10.1002/smll.201900046.

[222] Huang WC, Ying R, Wang W, Guo Y, He Y, Mo X, et al. A macroporous hydrogel dressing with enhanced antibacterial and anti-inflammatory capabilities for accelerated wound healing. Adv Funct Mater. 2020; 30: 2000644.

[223] Li M, Liang Y, He J, Zhang H, Guo B. Two-pronged strategy of biomechanically active and biochemically multifunctional hydrogel wound dressing to accelerate wound closure and wound healing. Chem Mater. 2020; 32: 9937-53.

[224] Lu H, Yuan L, Yu X, Wu C, He D, Deng J. Recent advances of on-demand dissolution of hydrogel dressings. Burns Trauma. 2018; 6: 35.

[225] Wang H, Liu Y, Cai K, Zhang B, Tang S, Zhang W, et al. Antibacterial polysaccharide-based hydrogel dressing containing plant essential oil for burn wound healing. Burns Trauma. 2021; 9: tkab041.

[226] Xu N, Yuan Y, Ding L, Li J, Jia J, Li Z, et al. Multifunctional chitosan/gelatin@tannic acid cryogels decorated with in situ reduced silver nanoparticles for wound healing. Burns Trauma. 2022; 10: tkac019.

[227] Han Z, Deng L, Chen S, Wang H, Huang Y. Zn(2+)-loaded adhesive bacterial cellulose hydrogel with angiogenic and antibacterial abilities for accelerating wound healing. Burns. Trauma. 2023; 11: tkac048.

[228] Li Y, Wang X, Fu YN, Wei Y, Zhao L, Tao L. Self-adapting hydrogel to improve the therapeutic effect in wound-healing. ACS Appl Mater Interfaces. 2018; 10: 26046-55.

[229] Lin F, Wang Z, Xiang L, Deng L, Cui W. Charge-guided micro/Nano-hydrogel microsphere for penetrating cartilage matrix. Adv Funct Mater. 2021; 31: 2107678.

[230] Liao H, Guo X, Wan P, Yu G. Conductive MXene nanocomposite Organohydrogel for flexible, healable, Low-temperature tolerant strain sensors. Adv Funct Mater. 2019; 29: 1904507.

[231] Wang T, Zhang Y, Liu Q, Cheng W, Wang X, Pan L, et al. A self-healable, highly stretchable, and solution Processable conductive polymer composite for ultrasensitive strain and pressure sensing. Adv Funct Mater. 2018; 28: 1705551.

[232] Lei H, Fan D. Conductive, adaptive, multifunctional hydrogel combined with electrical stimulation for deep wound repair. Chem Eng J. 2021; 421: 129578. https://doi.org/10.1016/j.cej.2021.129578.

[233] Qu J, Zhao X, Liang Y, Xu Y, Ma PX, Guo B. Degradable conductive injectable hydrogels as novel antibacterial, antioxidant wound dressings for wound healing. Chem Eng J. 2019; 362: 548-60.

[234] Lei H, Fan D. A combination therapy using electrical stimulation and adaptive, conductive hydrogels loaded with self-assembled Nanogels incorporating short interfering RNA promotes the repair of diabetic chronic wounds. Adv Sci (Weinh). 2022; 9: e2201425. https://doi.org/10.1002/advs.202201425.

[235] Hermenegildo B, Ribeiro C, Perez-Alvarez L, Vilas JL, Learmonth DA, Sousa RA, et al. Hydrogel-based magnetoelectric microenvironments for tissue stimulation. Colloids Surf B Biointerfaces. 2019; 181: 1041-7.

[236] Liang J, Zeng H, Qiao L, Jiang H, Ye Q, Wang Z, et al. 3D printed piezoelectric wound dressing with dual piezoelectric response models for scar-prevention wound healing. ACS Appl Mater Interfaces. 2022; 14: 30507-22.

[237] Du S, Zhou N, Gao Y, Xie G, Du H, Jiang H, et al. Bioinspired hybrid patches with self-adhesive hydrogel and piezoelectric nanogenerator for promoting skin wound healing. Nano Res. 2020; 13: 2525-33.

[238] Wang R, Li J, Chen W, Xu T, Yun S, Xu Z, et al. A biomimetic mussel-inspired ε-poly-l-lysine hydrogel with robust tissue-anchor and anti-infection capacity. Adv Funct Mater. 2017; 27: 1604894.

[239] Li Y, Fu R, Guan Y, Zhang Z, Yang F, Xiao C, et al. Piezoelectric hydrogel for prophylaxis and early treatment of pressure injuries/pressure ulcers. ACS Biomater Sci Eng. 2022; 8: 3078-86.

[240] Wang Z, Liu Z, Zhao G, Zhang Z, Zhao X, Wan X, et al. Stretchable unsymmetrical piezoelectric BaTiO3 composite hydrogel for triboelectric Nanogenerators and multimodal sensors. ACS Nano. 2022; 16: 1661-70.

[241] Ribeiro S, Gomes AC, Etxebarria I, Lanceros-Mendez S, Ribeiro C. Electroactive biomaterial surface engineering effects on muscle cells differentiation. Mater Sci Eng C Mater Biol Appl. 2018; 92: 868-74.

[242] Shima A, Morimoto Y, Sweeney HL, Takeuchi S. Three-dimensional contractile muscle tissue consisting of human skeletal myocyte cell line. Exp Cell Res. 2018; 370: 168-73.

[243] Ostrovidov S, Ebrahimi M, Bae H, Nguyen HK, Salehi S, Kim SB, et al. Gelatin-polyaniline composite nanofibers enhanced excitation-contraction coupling system maturation in Myotubes. ACS Appl Mater Interfaces. 2017; 9: 42444-58.

[244] Konuk Tokak E, Cetin Altindal D, Akdere OE, Gumusderelioglu M. In-vitro effectiveness of poly-beta-alanine reinforced poly(3-hydroxybutyrate) fibrous scaffolds for skeletal muscle regeneration. Mater Sci Eng C Mater Biol Appl. 2021; 131: 112528.

[245] Clayton RH, Bernus O, Cherry EM, Dierckx H, Fenton FH, Mirabella L, et al. Models of cardiac tissue electrophysiology: progress, challenges and open questions. Prog Biophys Mol Biol. 2011; 104: 22-48.

[246] Gouveia PJ, Rosa S, Ricotti L, Abecasis B, Almeida HV, Monteiro L, et al. Flexible nanofilms coated with aligned piezoelectric microfibers preserve the contractility of cardiomyocytes. Biomaterials. 2017; 139: 213-28.

[247] Liu X, Zhao H, Lu Y, Li S, Lin L, Du Y, et al. In vitro cardiomyocyte-driven biogenerator based on aligned piezoelectric nanofibers. Nanoscale. 2016; 8: 7278-86.

[248] Hitscherich P, Wu S, Gordan R, Xie LH, Arinzeh T, Lee EJ. The effect of PVDF-TrFE scaffolds on stem cell derived cardiovascular cells. Biotechnol Bioeng. 2016; 113: 1577-85.

[249] Adadi N, Yadid M, Gal I, Asulin M, Feiner R, Edri R, et al. Electrospun fibrous PVDF-TrFe scaffolds for cardiac tissue engineering, differentiation, and maturation. Advanced Materials Technologies. 2020; 5: 1900820.

[250] Augustine R, Dominic EA, Reju I, Kaimal B, Kalarikkal N, Thomas S. Investigation of angiogenesis and its mechanism using zinc oxide nanoparticle-loaded electrospun tissue engineering scaffolds. RSC Adv. 2014; 4: 51528-36.

[251] Kargozar S, Baino F, Hamzehlou S, Hill RG, Mozafari M. Bioactive glasses: sprouting angiogenesis in tissue engineering. Trends Biotechnol. 2018; 36: 430-44.

[252] Homaeigohar S, Li M, Boccaccini AR. Bioactive glass-based fibrous wound dressings. Burns Trauma. 2022; 10: tkac038.

[253] Li C, Zhang S, Yao Y, Wang Y, Xiao C, Yang B, et al. Piezoelectric bioactive glasses composite promotes angiogenesis by the synergistic effect of wireless electrical stimulation and active ions. Adv Healthc Mater. 2023; 12: e2300064. https://doi.org/10.1002/adhm.202300064.