Journal of Advanced Materials and Technologies

Journal of Advanced Materials and Technologies

An Overview of Innovate Approach Generating Electrical Stimulation via Electroactive Biomaterials for Cardiac Tissue Engineering

Document Type : Research Review Article

Authors
Elham Golafshan 1
Habib Nikukar 2
Shohreh Mashayekhan 3
Mohammad Ali Shokrgozar 4
Abdolreza Simchi 5
1 Ph.D. Candidate, Institute for Convergence Science and Technology, Center for Nanoscience and Nanotechnology, Sharif University of Technology, Tehran, Iran. Scool of Advanced Medical, Shahid Sadoughi University of Medical Sciences, Yazd, Iran.
2 Associate Professor, Biotechnology Research Center, Yazd Reproductive Sciences Institute, Shahid Sadoughi University of Medical Sciences, Yazd, Iran.
3 Associate Professor, Institute for Convergence Science and Technology, Center for Nanoscience and Nanotechnology, Sharif University of Technology, Tehran, Iran. Department of Chemical and Petroleum Engineering, Sharif University of Technology, Tehran, Iran.
4 Professor, National Cell Bank of Iran, Pasteur Institute of Iran, Tehran, Iran.
5 Professor, Institute for Convergence Science and Technology, Center for Nanoscience and Nanotechnology, Sharif University of Technology, Tehran, Iran. Department of Materials Science and Engineering, Sharif University of Technology, Tehran, Iran.
10.30501/jamt.2025.507009.1321
Abstract
Cardiovascular disease, particularly myocardial infarction, remains one of the leading causes of mortality worldwide. Despite advancements in treatment strategies, the clinical application of existing therapies is hindered by the impaired electrical and mechanical properties of damaged cardiac tissue. To address these challenges, researchers have explored the integration of stem cells with biomaterials to develop bio-mimetic engineered constructs in vitro. These constructs are essential for cardiac tissue regeneration, drug screening, and congenital heart disease research. During heart development, mechanical, chemical, and electrical signals contribute to enhanced cell-cell interactions, cellular alignment, and functional maturity. Among these stimuli, Electrical Stimulation (ES) has emerged as a promising intervention for cardiac tissue engineering. This review explores the role of endogenous bioelectrical signals in cardiac tissue and their impact on cellular processes such as adhesion, proliferation, alignment, migration, and differentiation in response to ES. In addition, we discuss the introduction of electroactive biomaterials (EABMs), which are capable of generating electrical signals, and the latest advancements in their application for cardiac tissue engineering. The final section highlights the current limitations of this approach and future prospects in the field.
Keywords
Conductive Biomaterials
Cardiac Tissue Engineering
Electrical Stimulation
Piezoelectric
Magnetoelectric
Triboelectric

Subjects

  1. Abbasipour, M., Khajavi, R., Yousefi, A. A., Yazdanshenas, M. E., & Razaghian, F. (2017). The piezoelectric response of electrospun PVDF nanofibers with graphene oxide, graphene, and halloysite nanofillers: a comparative study. Journal of Materials Science: Materials in Electronics, 28(21), 15942-15952. https://doi.org/10.1007/s10854-017-7491-4
  2. Abdelhalim, M. A. K. (2011). Exposure to gold nanoparticles produces cardiac tissue damage that depends on the size and duration of exposure. Lipids in health and disease, 10, 1-9. https://doi.org/10.1186/1476-511X-10-205
  3. Abedi, A., Bakhshandeh, B., Babaie, A., Mohammadnejad, J., Vahdat, S., Mombeiny, R., Moosavi, S. R., Amini, J., & Tayebi, L. (2021). Concurrent application of conductive biopolymeric chitosan/polyvinyl alcohol/MWCNTs nanofibers, intracellular signaling manipulating molecules and electrical stimulation for more effective cardiac tissue engineering. Materials Chemistry and Physics, 258, 123842. https://doi.org/10.1016/j.matchemphys.2020.123842
  4. Adadi, N., Yadid, M., Gal, I., Asulin, M., Feiner, R., Edri, R., & Dvir, T. (2020). Electrospun Fibrous PVDF‐TrFe Scaffolds for Cardiac Tissue Engineering, Differentiation, and Maturation. Advanced Materials Technologies, 5(3). https://doi.org/10.1002/admt.201900820
  5. Akiyama, H., Ito, A., Sato, M., Kawabe, Y., & Kamihira, M. (2010). Construction of cardiac tissue rings using a magnetic tissue fabrication technique. International Journal of molecular sciences, 11(8), 2910-2920. https://doi.org/10.3390/ijms11082910
  6. Alarcon, E. I., Udekwu, K. I., Noel, C. W., Gagnon, L. B. P., Taylor, P. K., Vulesevic, B., Simpson, M. J., Gkotzis, S., Islam, M. M., & Lee, C. J. (2015). Safety and efficacy of composite collagen–silver nanoparticle hydrogels as tissue engineering scaffolds. Nanoscale, 7(44), 18789-18798. https://doi.org/10.1039/C5NR03826J
  7. Allen, K., Bandl, A., Pachter, N., & Hookway, T. (2024). Short-term Electrical Stimulation Impacts Cardiac Cell Structure and Function. bioRxiv, 2024-05. https://doi.org/10.1101/2024.05.19.594880
  8. Allison, S., Ahumada, M., Andronic, C., McNeill, B., Variola, F., Griffith, M., Ruel, M., Hamel, V., Liang, W., & Suuronen, E. J. (2017). Electroconductive nanoengineered biomimetic hybrid fibers for cardiac tissue engineering. Journal of Materials Chemistry B, 5(13), 2402-2406. https://doi.org/10.1039/C7TB00405B
  9. Asaro, G. A., Solazzo, M., Suku, M., Spurling, D., Genoud, K., Gonzalez, J. G., Brien, F. J. O., Nicolosi, V., & Monaghan, M. G. (2023). MXene functionalized collagen biomaterials for cardiac tissue engineering driving iPSC-derived cardiomyocyte maturation. npj 2D Materials and Applications, 7(1), 44. https://doi.org/10.1038/s41699-023-00409-w
  10. Baei, P., Jalili-Firoozinezhad, S., Rajabi-Zeleti, S., Tafazzoli-Shadpour, M., Baharvand, H., & Aghdami, N. (2016). Electrically conductive gold nanoparticle-chitosan thermosensitive hydrogels for cardiac tissue engineering. Materials Science and Engineering: C, 63, 131-141. https://doi.org/10.1016/j.msec.2016.02.056
  11. Balint, R., Cassidy, N. J., & Cartmell, S. H. (2013). Electrical stimulation: a novel tool for tissue engineering. Tissue Engineering Part B: Reviews, 19(1), 48-57. https://doi.org/10.1089/ten.TEB.2012.0183
  12. Barras, F., Aussel, L., & Ezraty, B. (2018). Silver and antibiotic, new facts to an old story. Antibiotics, 7(3), 79. https://doi.org/10.3390/antibiotics7030079
  13. Baruscotti, M., Barbuti, A., & Bucchi, A. (2010). The cardiac pacemaker current. Journal of Molecular and Cellular Cardiology, 48(1), 55-64. https:/doi.org/10.1016/j.yjmcc.2009.06.019
  14. Basara, G., Saeidi-Javash, M., Ren, X., Bahcecioglu, G., Wyatt, B. C., Anasori, B., Zhang, Y., & Zorlutuna, P. (2022). Electrically conductive 3D printed Ti3C2Tx MXene-PEG composite constructs for cardiac tissue engineering. Acta biomaterialia, 139, 179-189. https://doi.org/10.1016/j.actbio.2020.12.033
  15. Benjamin, E. J., Muntner, P., Alonso, A., Bittencourt, M. S., Callaway, C. W., Carson, A. P., Chamberlain, A. M., Chang, A. R., Cheng, S., & Das, S. R. (2019). Heart disease and stroke statistics—2019 update: a report from the American Heart Association. Circulation, 139(10), e56-e528. https://doi.org/10.1161/CIR.0000000000000659
  16. Bertuoli, P. T., Ordono, J., Armelin, E., Perez-Amodio, S., Baldissera, A. F., Ferreira, C. A., Puiggali, J., Engel, E., Del Valle, L. J., & Aleman, C. (2019). Electrospun Conducting and Biocompatible Uniaxial and Core-Shell Fibers Having Poly(lactic acid), Poly(ethylene glycol), and Polyaniline for Cardiac Tissue Engineering. ACS Omega, 4(2), 3660-3672. https://doi.org/10.1021/acsomega.8b03411
  17. Buzsaki, G., & Draguhn, A. (2004). Neuronal oscillations in cortical networks. science, 304(5679), 1926-1929. https://doi.org/10.1126/science.1099745
  18. Cafarelli, A., Marino, A., Vannozzi, L., Puigmartí-Luis, J., Pané, S., Ciofani, G., & Ricotti, L. (2021). Piezoelectric nanomaterials activated by ultrasound: the pathway from discovery to future clinical adoption. ACS nano, 15(7), 11066-11086. https://doi.org/10.1021/acsnano.1c03087
  19. Cahill, T. J., Choudhury, R. P., & Riley, P. R. (2017). Heart regeneration and repair after myocardial infarction: translational opportunities for novel therapeutics. Nature reviews Drug discovery, 16(10), 699-717. https://doi.org/10.1038/nrd.2017.106
  20. Chahal, A. A., & Somers, V. K. (2016). Ion Channel Remodeling—A Potential Mechanism Linking Sleep Apnea and Sudden Cardiac Death. Journal of the American Heart Association, 5(8), e004195. https://doi.org/doi:10.1161/JAHA.116.004195
  21. Chithrani, B. D., Ghazani, A. A., & Chan, W. C. (2006). Determining the size and shape dependence of gold nanoparticle uptake into mammalian cells. Nano letters, 6(4), 662-668. https://doi.org/10.1021/nl052396o
  22. Chorsi, M. T., Curry, E. J., Chorsi, H. T., Das, R., Baroody, J., Purohit, P. K., Ilies, H., & Nguyen, T. D. (2019). Piezoelectric biomaterials for sensors and actuators. Advanced Materials, 31(1), 1802084. https://doi.org/10.1002/adma.201802084
  23. Cui, H., Liu, Y., Cheng, Y., Zhang, Z., Zhang, P., Chen, X., & Wei, Y. (2014). In vitro study of electroactive tetraaniline-containing thermosensitive hydrogels for cardiac tissue engineering. Biomacromolecules, 15(4), 1115-1123. https://doi.org/10.1021/bm4018963
  24. da Silva, L. P., Kundu, S. C., Reis, R. L., & Correlo, V. M. (2020). Electric phenomenon: A disregarded tool in tissue engineering and regenerative medicine. Trends in biotechnology, 38(1), 24-49. https://doi.org/10.1016/j.tibtech.2019.07.002
  25. Del Valle, L., Aradilla, D., Oliver, R., Sepulcre, F., Gamez, A., Armelin, E., Alemán, C., & Estrany, F. (2007). Cellular adhesion and proliferation on poly (3, 4-ethylenedioxythiophene): benefits in the electroactivity of the conducting polymer. European Polymer Journal, 43(6), 2342-2349. https://doi.org/10.1016/j.eurpolymj.2007.03.050
  26. Deng, W., Yang, T., Jin, L., Yan, C., Huang, H., Chu, X., Wang, Z., Xiong, D., Tian, G., & Gao, Y. (2019). Cowpea-structured PVDF/ZnO nanofibers based flexible self-powered piezoelectric bending motion sensor towards remote control of gestures. Nano Energy, 55, 516-525. https://doi.org/10.1016/j.nanoen.2018.10.049
  27. Diedkova, K., Pogrebnjak, A. D., Kyrylenko, S., Smyrnova, K., Buranich, V. V., Horodek, P., Zukowski, P., Koltunowicz, T. N., Galaszkiewicz, P., Makashina, K., Bondariev, V., Sahul, M., Čaplovičová, M., Husak, Y., Simka, W., Korniienko, V., Stolarczyk, A., Blacha-Grzechnik, A., Balitskyi, V., Zahorodna, V., Baginskiy, I., Riekstina, U., Gogotsi, O., Gogotsi, Y., & Pogorielov, M. (2023). Polycaprolactone–MXene Nanofibrous Scaffolds for Tissue Engineering. ACS Applied Materials & Interfaces, 15(11), 14033-14047. https://doi.org/10.1021/acsami.2c22780
  28. Dong, C., Fu, Y., Zang, W., He, H., Xing, L., & Xue, X. (2017). Self-powering/self-cleaning electronic-skin basing on PVDF/TiO2 nanofibers for actively detecting body motion and degrading organic pollutants. Applied Surface Science, 416, 424-431. https:/doi.org/10.1016/j.apsusc.2017.04.188
  29. Doustvandi, B., Imani, R., & Yousefzadeh, M. (2023). Study of Electrospun PVDF/GO Nanofibers as a Conductive Piezoelectric Heart Patch for Potential Support of Myocardial Regeneration. Macromolecular Materials and Engineering, 309(1), 2300243. https://doi.org/10.1002/mame.202300243
  30. Dozois, M. D., Bahlmann, L. C., Zilberman, Y., & Tang, X. (2017). Carbon nanomaterial-enhanced scaffolds for the creation of cardiac tissue constructs: A new frontier in cardiac tissue engineering. Carbon, 120, 338-349. https:/doi.org/10.1016/j.carbon.2017.05.050
  31. Ebad, M., & Vahidi, B. (2022). In silico analysis of stem cells mechanical stimulations for mechnoregulation toward cardiomyocytes. International Journal of Engineering, Transactions B: Applications, 35(10.5829). https://doi.org/10.5829/ije.2022.35.11b.18
  32. Esmaeili, H., Patino-Guerrero, A., Hasany, M., Ansari, M. O., Memic, A., Dolatshahi-Pirouz, A., & Nikkhah, M. (2022). Electroconductive biomaterials for cardiac tissue engineering. Acta biomaterialia, 139, 118-140. https://doi.org/10.1016/j.actbio.2021.08.031
  33. Esmaeili, H., Patino-Guerrero, A., Nelson, R. A., Jr., Karamanova, N., T, M. F., Zhu, W., Perreault, F., Migrino, R. Q., & Nikkhah, M. (2024). Engineered Gold and Silica Nanoparticle-Incorporated Hydrogel Scaffolds for Human Stem Cell-Derived Cardiac Tissue Engineering. ACS Biomater Sci Eng, 10(4), 2351-2366. https://doi.org/10.1021/acsbiomaterials.3c01256
  34. Fan, F. R., Tian, Z. Q., & Lin Wang, Z. (2012). Flexible triboelectric generator. Nano Energy, 1(2), 328-334. https:/doi.org/10.1016/j.nanoen.2012.01.004
  35. Ferson, N. D., Uhl, A. M., & Andrew, J. S. (2021). Piezoelectric and Magnetoelectric Scaffolds for Tissue Regeneration and Biomedicine: A Review. IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control, 68(2), 229-241. https://doi.org/10.1109/TUFFC.2020.3020283
  36. Fotouhi Ardakani, F., Mohammadi, M., & Mashayekhan, S. (2022). ZnO-incorporated polyvinylidene fluoride/poly(ε-caprolactone) nanocomposite scaffold with controlled release of dexamethasone for bone tissue engineering. Applied Physics A, 128(8), 654. https://doi.org/10.1007/s00339-022-05762-z
  37. Ganji, Y., Li, Q., Quabius, E. S., Böttner, M., Selhuber-Unkel, C., & Kasra, M. (2016). Cardiomyocyte behavior on biodegradable polyurethane/gold nanocomposite scaffolds under electrical stimulation. Materials Science and Engineering: C, 59, 10-18. https://doi.org/10.1016/j.msec.2015.09.074
  38. Ghovvati, M., Kharaziha, M., Ardehali, R., & Annabi, N. (2022). Recent advances in designing electroconductive biomaterials for cardiac tissue engineering. Advanced healthcare materials, 11(13), 2200055. https://doi.org/10.1002/adhm.202200055
  39. Gil-Castell, O., Ontoria-Oviedo, I., Badia, J., Amaro-Prellezo, E., Sepúlveda, P., & Ribes-Greus, A. (2022). Conductive polycaprolactone/gelatin/polyaniline nanofibres as functional scaffolds for cardiac tissue regeneration. Reactive and Functional Polymers, 170, 105064. https://doi.org/10.1016/j.reactfunctpolym.2021.105064
  40. Golafshan, E., Nikukar, H., Mashayekhan, S., Shokrgozar, M. A., & Simchi, A. (2024). PVDF-Modified Graphene Nanosheets as a Piezoelectric and Electroconductive Bilayer Platform for Cardiac Cell Stimulation. ACS Applied Nano Materials, 7(18), 21778-21790. https://doi.org/10.1021/acsanm.4c03749
  41. Guo, B., & Ma, P. X. (2018). Conducting polymers for tissue engineering. Biomacromolecules, 19(6), 1764-1782. https://doi.org/10.1021/acs.biomac.8b00276
  42. Hendrickson, T., Mancino, C., Whitney, L., Tsao, C., Rahimi, M., & Taraballi, F. (2021). Mimicking cardiac tissue complexity through physical cues: A review on cardiac tissue engineering approaches. Nanomedicine: Nanotechnology, Biology and Medicine, 33, 102367. https:/doi.org/10.1016/j.nano.2021.102367
  43. Hitscherich, P., Wu, S., Gordan, R., Xie, L. H., Arinzeh, T., & Lee, E. J. (2016). The effect of PVDF-TrFE scaffolds on stem cell derived cardiovascular cells. Biotechnology Bioengineering, 113(7), 1577-1585. https://doi.org/10.1002/bit.25918
  44. Hitscherich, P., Aphale, A., Gordan, R., Whitaker, R., Singh, P., Xie, L. H., Patra, P., & Lee, E. J. (2018). Electroactive graphene composite scaffolds for cardiac tissue engineering. Journal of Biomedical Materials Research Part A, 106(11), 2923-2933. https://doi.org/10.1002/jbm.a.36481
  45. Hosoyama, K., Ahumada, M., McTiernan, C. D., Davis, D. R., Variola, F., Ruel, M., Liang, W., Suuronen, E. J., & Alarcon, E. I. (2018). Nanoengineered electroconductive collagen-based cardiac patch for infarcted myocardium repair. ACS applied materials & interfaces, 10(51), 44668-44677. https://doi.org/10.1021/acsami.8b18844
  46. Izadifar, M., Chapman, D., Babyn, P., Chen, X., & Kelly, M. E. (2018). UV-assisted 3D bioprinting of nanoreinforced hybrid cardiac patch for myocardial tissue engineering. Tissue Engineering Part C: Methods, 24(2), 74-88. https://doi.org/10.1089/ten.tec.2017.0346
  47. Jacob, J., More, N., Kalia, K., & Kapusetti, G. (2018). Piezoelectric smart biomaterials for bone and cartilage tissue engineering. Inflammation and regeneration, 38(1), 2. https://doi.org/10.1186/s41232-018-0059-8
  48. Jiang, W., Li, H., Liu, Z., Li, Z., Tian, J., Shi, B., Zou, Y., Ouyang, H., Zhao, C., Zhao, L., Sun, R., Zheng, H., Fan, Y., Wang, Z. L., & Li, Z. (2018). Fully Bioabsorbable Natural-Materials-Based Triboelectric Nanogenerators. Advance Materials, 30(32), e1801895. https://doi.org/10.1002/adma.201801895
  49. Jiang, L., Chen, D., Wang, Z., Zhang, Z., Xia, Y., Xue, H., & Liu, Y. (2019). Preparation of an electrically conductive graphene oxide/chitosan scaffold for cardiac tissue engineering. Applied biochemistry and biotechnology, 188(4), 952-964. https://doi.org/10.1007/s12010-019-02967-6
  50. Jing, T., Tao, X., Li, T., Li, Z., Zhang, H., Huang, G., Jin, Z., Xu, J., Xie, C., & Qu, S. (2024). Magnetostriction enhanced self-powered nanofiber sheet as cardiac patch with magnetoelectric synergistic effect on actuating Na+ k+-ATPase. Chemical Engineering Journal, 490, 151791. https://doi.org/10.1016/j.cej.2024.151791
  51. Kabir, H., Kamali Dehghan, H., Mashayekhan, S., Bagherzadeh, R., & Sorayani Bafqi, M. S. (2022). Hybrid fibrous (PVDF-BaTiO3)/ PA-11 piezoelectric patch as an energy harvester for pacemakers. Journal of Industrial Textiles, 51(3_suppl), 4698S-4719S. https://doi.org/10.1177/15280837211057575
  52. Kai, D., Prabhakaran, M. P., Jin, G., & Ramakrishna, S. (2011). Polypyrrole‐contained electrospun conductive nanofibrous membranes for cardiac tissue engineering. Journal of biomedical materials research Part A, 99(3), 376-385. https://doi.org/10.1002/jbm.a.33200
  53. Kayser, L. V., & Lipomi, D. J. (2019). Stretchable Conductive Polymers and Composites Based on PEDOT and PEDOT:PSS. Advance Materials, 31(10), e1806133. https://doi.org/10.1002/adma.201806133
  54. Kazemi, M., Chogan, F., Rezaian, A. H., Mehdi Nawaz Eghmad, R. A., & Ahmadi Tafti, S. (2022). Injectable Thermosensitive Hydrogel (Chitosan/Gelatin/β-Glycerol Phosphate) Reinforced with Polyaniline/Carboxylated Carbon Nanotube/Gelatin Containing Stem Cells for Cardiac Tissue Engineering. Journal of Advanced Materials and Technologies, 11(2), 71-87. [In Persian]. https://doi.org/10.30501/jamt.2023.311513.1199
  55. Khalil, A. K., Fouad, H., Abdal-hay, A., Abd El-salam, N. M., & Abdelrazek Khalil, K. (2023). Fabrication and Characterization of Piezoelectric PEO/SF/BaTiO3 Scaffolds for Cardiac Tissue Engineering. Journal of Composites Science, 7(5), 200. https://doi.org/10.3390/jcs7050200
  56. Kharaziha, M., Shin, S. R., Nikkhah, M., Topkaya, S. N., Masoumi, N., Annabi, N., Dokmeci, M. R., & Khademhosseini, A. (2014). Tough and flexible CNT-polymeric hybrid scaffolds for engineering cardiac constructs. Biomaterials, 35(26), 7346-7354. https://doi.org/10.1016/j.biomaterials.2014.05.014
  57. Kinloch, I. A., Suhr, J., Lou, J., Young, R. J., & Ajayan, P. M. (2018). Composites with carbon nanotubes and graphene: An outlook. Science, 362(6414), 547-553. https://doi.org/10.1126/science.aat7439
  58. Koohkhezri, M., Lotfi, R., Zandi, N., Emami, Z., Tamjid, E., & Simchi, A. (2024). Drug-Eluting and Antibacterial Core–Shell Polycaprolactone/Pectin Nanofibers Containing Ti3C2T x MXene and Medical Herbs for Wound Dressings. ACS Applied Bio Materials, 7(11), 7244-7255. https://doi.org/10.1021/acsabm.4c00880
  59. Kopyl, S., Surmenev, R., Surmeneva, M., Fetisov, Y., & Kholkin, A. (2021). Magnetoelectric effect: principles and applications in biology and medicine– a review. Materials Today Bio, 12, 100149. https:/doi.org/10.1016/j.mtbio.2021.100149
  60. Kota, A. K., Cipriano, B. H., Duesterberg, M. K., Gershon, A. L., Powell, D., Raghavan, S. R., & Bruck, H. A. (2007). Electrical and rheological percolation in polystyrene/MWCNT nanocomposites. Macromolecules, 40(20), 7400-7406. https://doi.org/10.1021/ma0711792
  61. Lalegül-Ülker, Ö., Elçin, A. E., & Elçin, Y. M. (2018). Intrinsically conductive polymer nanocomposites for cellular applications. Cutting-edge enabling technologies for regenerative medicine, 135-153. https://doi.org/10.1007/978-981-13-0950-2_8
  62. Lee, J., Manoharan, V., Cheung, L., Lee, S., Cha, B.-H., Newman, P., Farzad, R., Mehrotra, S., Zhang, K., & Khan, F. (2019). Nanoparticle-based hybrid scaffolds for deciphering the role of multimodal cues in cardiac tissue engineering. ACS nano, 13(11), 12525-12539. https://doi.org/10.1021/acsnano.9b03050
  63. Li, Y., Li, X., Zhao, R., Wang, C., Qiu, F., Sun, B., Ji, H., Qiu, J., & Wang, C. (2017). Enhanced adhesion and proliferation of human umbilical vein endothelial cells on conductive PANI-PCL fiber scaffold by electrical stimulation. Materials Science and Engineering: C, 72, 106-112. https://doi.org/10.1016/j.msec.2016.11.052
  64. Li, Y., Liao, C., & Tjong, S. C. (2019). Electrospun polyvinylidene fluoride-based fibrous scaffolds with piezoelectric characteristics for bone and neural tissue engineering. Nanomaterials, 9(7), 952. https://doi.org/10.3390/nano9070952
  65. Liaw, N. Y., & Zimmermann, W. H. (2016). Mechanical stimulation in the engineering of heart muscle. Adv Drug Deliv Rev, 96, 156-160. https://doi.org/10.1016/j.addr.2015.09.001
  66. Liu, Z., Davis, C., Cai, W., He, L., Chen, X., & Dai, H. (2008). Circulation and long-term fate of functionalized, biocompatible single-walled carbon nanotubes in mice probed by Raman spectroscopy. Proceedings of the National Academy of Sciences, 105(5), 1410-1415. https://doi.org/10.1073/pnas.0707654105
  67. Liu, X., Ma, J., Wu, X., Lin, L., & Wang, X. (2017). Polymeric Nanofibers with Ultrahigh Piezoelectricity via Self-Orientation of Nanocrystals. ACS Nano, 11(2), 1901-1910. https://doi.org/10.1021/acsnano.6b07961
  68. Liu, Z., Wan, X., Wang, Z. L., & Li, L. (2021). Electroactive biomaterials and systems for cell fate determination and tissue regeneration: design and applications. Advanced Materials, 33(32), 2007429. https://doi.org/10.1002/adma.202007429
  69. Lotfi, R., Zandi, N., Pourjavadi, A., Christiansen, J. d. C., Gurevich, L., Mehrali, M., Dolatshahi-Pirouz, A., Pennisi, C. P., Tamjid, E., & Simchi, A. (2023). Engineering photo-cross-linkable MXene-based hydrogels: durable conductive biomaterials for electroactive tissues and interfaces. ACS Biomaterials Science & Engineering, 10(2), 800-813. https://doi.org/10.1021/acsbiomaterials.3c01394
  70. Ma, B., Liu, F., Li, Z., Duan, J., Kong, Y., Hao, M., Ge, S., Jiang, H., & Liu, H. (2019). Piezoelectric nylon-11 nanoparticles with ultrasound assistance for high-efficiency promotion of stem cell osteogenic differentiation. Journal of materials chemistry B, 7(11), 1847-1854. https://doi.org/10.1039/C8TB03321H
  71. Macário, D., Domingos, I., Carvalho, N., Pinho, P., & Alves, H. (2022). Harvesting circuits for triboelectric nanogenerators for wearable applications. iScience, 25(4), 103977. https:/doi.org/10.1016/j.isci.2022.103977
  72. Maiti, D., Tong, X., Mou, X., & Yang, K. (2019). Carbon-based nanomaterials for biomedical applications: a recent study. Frontiers in pharmacology, 9, 430833. https://doi.org/10.3389/fphar.2018.01401
  73. Marino, A., Bargero, A., & Ciofani, G. (2024). Piezoelectric nanomaterials: latest applications in biomedicine and challenges in clinical translation. Nanomedicine(0). https://doi.org/10.2217/nnm-2024-0080
  74. Martinelli, V., Cellot, G., Toma, F. M., Long, C. S., Caldwell, J. H., Zentilin, L., Giacca, M., Turco, A., Prato, M., & Ballerini, L. (2012). Carbon nanotubes promote growth and spontaneous electrical activity in cultured cardiac myocytes. Nano letters, 12(4), 1831-1838. https://doi.org/10.1021/nl204064s
  75. Mehrotra, S., Dey, S., Sachdeva, K., Mohanty, S., & Mandal, B. B. (2023). Recent advances in tailoring stimuli-responsive hybrid scaffolds for cardiac tissue engineering and allied applications. Journal of Materials Chemistry B, 11(43), 10297-10331. https://doi.org/10.1039/D3TB00450C
  76. Meira, R. M., Ribeiro, S., Irastorza, I., Silvan, U., Lanceros-Mendez, S., & Ribeiro, C. (2024). Electroactive poly(vinylidene fluoride-trifluoroethylene)/graphene composites for cardiac tissue engineering applications. J Colloid Interface Sci, 663, 73-81. https://doi.org/10.1016/j.jcis.2024.02.139
  77. Mody, V. V., Siwale, R., Singh, A., & Mody, H. R. (2010). Introduction to metallic nanoparticles. Journal of Pharmacy and bioallied sciences, 2(4), 282-289. https://doi.org/10.4103/0975-7406.72127
  78. Moghadam, B. H., Hasanzadeh, M., & Simchi, A. (2020). Self-Powered Wearable Piezoelectric Sensors Based on Polymer Nanofiber–Metal–Organic Framework Nanoparticle Composites for Arterial Pulse Monitoring. ACS Applied Nano Materials, 3(9), 8742-8752. https://doi.org/10.1021/acsanm.0c01551
  79. Mombini, S., Mohammadnejad, J., Bakhshandeh, B., Narmani, A., Nourmohammadi, J., Vahdat, S., & Zirak, S. (2019). Chitosan-PVA-CNT nanofibers as electrically conductive scaffolds for cardiovascular tissue engineering. International journal of biological macromolecules, 140, 278-287. https://doi.org/10.1016/j.ijbiomac.2019.08.046
  80. Mota, M. L., Carrillo, A., Verdugo, A. J., Olivas, A., Guerrero, J. M., De la Cruz, E. C., & Noriega Ramírez, N. (2019). Synthesis and novel purification process of PANI and PANI/AgNPs composite. Molecules, 24(8), 1621. https://doi.org/10.3390/molecules24081621
  81. Mousavi, A., Mashayekhan, S., Baheiraei, N., & Pourjavadi, A. (2021). Biohybrid oxidized alginate/myocardial extracellular matrix injectable hydrogels with improved electromechanical properties for cardiac tissue engineering. International Journal of Biological Macromolecules, 180, 692-708. https:/doi.org/10.1016/j.ijbiomac.2021.03.097
  82. Najjari, A., Mehdinavaz Aghdam, R., Ebrahimi, S. S., Suresh K, S., Krishnan, S., Shanthi, C., & Ramalingam, M. (2022). Smart piezoelectric biomaterials for tissue engineering and regenerative medicine: A review. Biomedical Engineering/Biomedizinische Technik, 67(2), 71-88. https://doi.org/10.1515/bmt-2021-0265
  83. Nezakati, T., Seifalian, A., Tan, A., & Seifalian, A. M. (2018). Conductive polymers: opportunities and challenges in biomedical applications. Chemical reviews, 118(14), 6766-6843. https://doi.org/10.1021/acs.chemrev.6b00275
  84. Ning, C., Zhou, Z., Tan, G., Zhu, Y., & Mao, C. (2018). Electroactive polymers for tissue regeneration: Developments and perspectives. Progress in polymer science, 81, 144-162. https://doi.org/10.1016/j.progpolymsci.2018.01.001
  85. Norahan, M. H., Amroon, M., Ghahremanzadeh, R., Mahmoodi, M., & Baheiraei, N. (2019a). Electroactive graphene oxide-incorporated collagen assisting vascularization for cardiac tissue engineering. J Biomed Mater Res A, 107(1), 204-219. https://doi.org/10.1002/jbm.a.36555
  86. Norahan, M. H., Pourmokhtari, M., Saeb, M. R., Bakhshi, B., Soufi Zomorrod, M., & Baheiraei, N. (2019b). Electroactive cardiac patch containing reduced graphene oxide with potential antibacterial properties. Materials Science and Engineering: C, 104, 109921. https:/doi.org/10.1016/j.msec.2019.109921
  87. Ovcharenko, E. A., Seifalian, A., Rezvova, M. A., Klyshnikov, K. Y., Glushkova, T. V., Akenteva, T. N., Antonova, L. V., Velikanova, E. A., Chernonosova, V. S., & Shevelev, G. Y. (2020). A new nanocomposite copolymer based on functionalised graphene oxide for development of heart valves. Scientific Reports, 10(1), 5271. https://doi.org/10.1038/s41598-020-62122-8
  88. Padala, S. K., Cabrera, J. A., & Ellenbogen, K. A. (2021). Anatomy of the cardiac conduction system. Pacing and Clinical Electrophysiology, 44(1), 15-25. https://doi.org/10.1111/pace.14107
  89. Parchehbaf-Kashani, M., Sepantafar, M., Talkhabi, M., Sayahpour, F. A., Baharvand, H., Pahlavan, S., & Rajabi, S. (2020). Design and characterization of an electroconductive scaffold for cardiomyocytes based biomedical assays. Materials Science and Engineering: C, 109, 110603. https:/doi.org/10.1016/j.msec.2019.110603
  90. Pilato, S., Moffa, S., Siani, G., Diomede, F., Trubiani, O., Pizzicannella, J., Capista, D., Passacantando, M., Samori, P., & Fontana, A. (2023). 3D Graphene Oxide-Polyethylenimine Scaffolds for Cardiac Tissue Engineering. ACS Appl Mater Interfaces, 15(11), 14077-14088. https://doi.org/10.1021/acsami.3c00216
  91. Qazi, T. H., Rai, R., & Boccaccini, A. R. (2014a). Tissue engineering of electrically responsive tissues using polyaniline based polymers: A review. Biomaterials, 35(33), 9068-9086. https://doi.org/10.1016/j.biomaterials.2014.07.020
  92. Qazi, T. H., Rai, R., Dippold, D., Roether, J. E., Schubert, D. W., Rosellini, E., Barbani, N., & Boccaccini, A. R. (2014b). Development and characterization of novel electrically conductive PANI–PGS composites for cardiac tissue engineering applications. Acta biomaterialia, 10(6), 2434-2445. https://doi.org/10.1016/j.actbio.2014.02.023
  93. Qi, F., Gao, X., Shuai, Y., Peng, S., Deng, Y., Yang, S., Yang, Y., & Shuai, C. (2022). Magnetic-driven wireless electrical stimulation in a scaffold. Composites Part B: Engineering, 237, 109864. https://doi.org/10.1016/j.compositesb.2022.109864
  94. Radisic, M., Park, H., Shing, H., Consi, T., Schoen, F. J., Langer, R., Freed, L. E., & Vunjak-Novakovic, G. (2004). Functional assembly of engineered myocardium by electrical stimulation of cardiac myocytes cultured on scaffolds. Proceedings of the National Academy of Sciences, 101(52), 18129-18134. https://doi.org/10.1073/pnas.0407817101
  95. Ribeiro, C., Costa, C. M., Correia, D. M., Nunes-Pereira, J., Oliveira, J., Martins, P., Goncalves, R., Cardoso, V. F., & Lanceros-Mendez, S. (2018). Electroactive poly(vinylidene fluoride)-based structures for advanced applications. Nat Protoc, 13(4), 681-704. https://doi.org/10.1038/nprot.2017.157
  96. Ribeiro, S., Ribeiro, C., Carvalho, E. O., Tubio, C. R., Castro, N., Pereira, N., Correia, V., Gomes, A. C., & Lanceros-Méndez, S. (2020). Magnetically activated electroactive microenvironments for skeletal muscle tissue regeneration. ACS Applied Bio Materials, 3(7), 4239-4252. https://doi.org/10.1021/acsabm.0c00315
  97. Roacho-Perez, J. A., Santoyo-Suarez, M. G., Quiroz-Reyes, A. G., Garza-Treviño, E. N., Islas, J. F., & Haider, K. H. (2024). Current Developments of Electroconductive Scaffolds for Cardiac Tissue Engineering. In K. H. Haider (Ed.), Handbook of Stem Cell Applications (pp. 911-938). Springer Nature Singapore. https://doi.org/10.1007/978-981-99-7119-0_55
  98. Roberts-Thomson, K. C., Kistler, P. M., Sanders, P., Morton, J. B., Haqqani, H. M., Stevenson, I., Vohra, J. K., Sparks, P. B., & Kalman, J. M. (2009). Fractionated atrial electrograms during sinus rhythm: relationship to age, voltage, and conduction velocity. Heart rhythm, 6(5), 587-591. https://doi.org/10.1016/j.hrthm.2009.02.023
  99. Roshanbinfar, K., Vogt, L., Greber, B., Diecke, S., Boccaccini, A. R., Scheibel, T., & Engel, F. B. (2018). Electroconductive biohybrid hydrogel for enhanced maturation and beating properties of engineered cardiac tissues. Advanced Functional Materials, 28(42), 1803951. https://doi.org/10.1002/adfm.201803951
  100. Roshanbinfar, K., Vogt, L., Ruther, F., Roether, J. A., Boccaccini, A. R., & Engel, F. B. (2020). Nanofibrous composite with tailorable electrical and mechanical properties for cardiac tissue engineering. Advanced Functional Materials, 30(7), 1908612. https://doi.org/10.1002/adfm.201908612
  101. Sapir, Y., Polyak, B., & Cohen, S. (2014). Cardiac tissue engineering in magnetically actuated scaffolds. Nanotechnology, 25(1), 014009. https://doi.org/10.1088/0957-4484/25/1/014009
  102. Satin, J., Kehat, I., Caspi, O., Huber, I., Arbel, G., Itzhaki, I., Magyar, J., Schroder, E. A., Perlman, I., & Gepstein, L. (2004). Mechanism of spontaneous excitability in human embryonic stem cell derived cardiomyocytes. The Journal of physiology, 559(2), 479-496. https://doi.org/10.1113/jphysiol.2004.068213
  103. Scuderi, G. J., & Butcher, J. (2017). Naturally Engineered Maturation of Cardiomyocytes. Front Cell Dev Biol, 5, 50. https://doi.org/10.3389/fcell.2017.00050
  104. Sencadas, V., Garvey, C., Mudie, S., Kirkensgaard, J. J., Gouadec, G., & Hauser, S. (2019). Electroactive properties of electrospun silk fibroin for energy harvesting applications. Nano Energy, 66, 104106. https://doi.org/10.1016/j.nanoen.2019.104106
  105. Shevach, M., Fleischer, S., Shapira, A., & Dvir, T. (2014). Gold nanoparticle-decellularized matrix hybrids for cardiac tissue engineering. Nano letters, 14(10), 5792-5796. https://doi.org/10.1021/nl502673m
  106. Shin, S. R., Jung, S. M., Zalabany, M., Kim, K., Zorlutuna, P., Kim, S. b., Nikkhah, M., Khabiry, M., Azize, M., & Kong, J. (2013). Carbon-nanotube-embedded hydrogel sheets for engineering cardiac constructs and bioactuators. ACS nano, 7(3), 2369-2380. https://doi.org/10.1021/nn305559j
  107. Shin, S. R., Zihlmann, C., Akbari, M., Assawes, P., Cheung, L., Zhang, K., Manoharan, V., Zhang, Y. S., Yüksekkaya, M., & Wan, K. t. (2016). Reduced graphene oxide‐gelMA hybrid hydrogels as scaffolds for cardiac tissue engineering. Small, 12(27), 3677-3689. https://doi.org/10.1002/smll.201600178
  108. Sirivisoot, S., Pareta, R., & Harrison, B. S. (2014). Protocol and cell responses in three-dimensional conductive collagen gel scaffolds with conductive polymer nanofibres for tissue regeneration. Interface focus, 4(1), 20130050. https://doi.org/10.1098/rsfs.2013.0050
  109. Song, C., Zhang, X., Wang, L., Wen, F., Xu, K., Xiong, W., Li, C., Li, B., Wang, Q., Xing, M. M. Q., & Qiu, X. (2019). An Injectable Conductive Three-Dimensional Elastic Network by Tangled Surgical-Suture Spring for Heart Repair. ACS Nano, 13(12), 14122-14137. https://doi.org/10.1021/acsnano.9b06761
  110. Spearman, B. S., Hodge, A. J., Porter, J. L., Hardy, J. G., Davis, Z. D., Xu, T., Zhang, X., Schmidt, C. E., Hamilton, M. C., & Lipke, E. A. (2015). Conductive interpenetrating networks of polypyrrole and polycaprolactone encourage electrophysiological development of cardiac cells. Acta biomaterialia, 28, 109-120. https://doi.org/10.1016/j.actbio.2015.09.025
  111. Srinivasan, S. Y., Cler, M., Zapata-Arteaga, O., Dorling, B., Campoy-Quiles, M., Martinez, E., Engel, E., Perez-Amodio, S., & Laromaine, A. (2023). Conductive Bacterial Nanocellulose-Polypyrrole Patches Promote Cardiomyocyte Differentiation. ACS Appllied Bio Materials, 6(7), 2860-2874. https://doi.org/10.1021/acsabm.3c00303
  112. Suh, T. C., Twiddy, J., Mahmood, N., Ali, K. M., Lubna, M. M., Bradford, P. D., Daniele, M. A., & Gluck, J. M. (2022). Electrospun Carbon Nanotube-Based Scaffolds Exhibit High Conductivity and Cytocompatibility for Tissue Engineering Applications. ACS Omega, 7(23), 20006-20019. https://doi.org/10.1021/acsomega.2c01807
  113. Tai, Y., Yang, S., Yu, S., Banerjee, A., Myung, N. V., & Nam, J. (2021). Modulation of piezoelectric properties in electrospun PLLA nanofibers for application-specific self-powered stem cell culture platforms. Nano Energy, 89, 106444. https://doi.org/10.1016/j.nanoen.2021.106444
  114. Talebi, A., Labbaf, S., & Karimzadeh, F. (2019). A conductive film of chitosan-polycaprolcatone-polypyrrole with potential in heart patch application. Polymer Testing, 75, 254-261. https://doi.org/10.1016/j.polymertesting.2019.02.029
  115. Tohidi, H., Maleki-Jirsaraei, N., Simchi, A., Mohandes, F., Emami, Z., Fassina, L., Naro, F., Conti, B., & Barbagallo, F. (2022). An Electroconductive, Thermosensitive, and Injectable Chitosan/Pluronic/Gold-Decorated Cellulose Nanofiber Hydrogel as an Efficient Carrier for Regeneration of Cardiac Tissue. Materials (Basel), 15(15). https://doi.org/10.3390/ma15155122
  116. Tohidi, H., Maleki, N., & Simchi, A. (2024). Conductive, injectable, and self-healing collagen-hyaluronic acid hydrogels loaded with bacterial cellulose and gold nanoparticles for heart tissue engineering. International J ournal Biology Macromolucle, 280(Pt 2), 135749. https://doi.org/10.1016/j.ijbiomac.2024.135749
  117. Tonelli, F. M., Santos, A. K., Gomes, K. N., Lorencon, E., Guatimosim, S., Ladeira, L. O., & Resende, R. R. (2012). Carbon nanotube interaction with extracellular matrix proteins producing scaffolds for tissue engineering. International Journal Nanomedicine, 7, 4511-4529. https://doi.org/10.2147/IJN.S33612
  118. Tsien, R., & Carpenter, D. (1978). Ionic mechanisms of pacemaker activity in cardiac Purkinje fibers. Federation Proceedings (Vol. 37, No. 8, pp. 2127-2131). https://pubmed.ncbi.nlm.nih.gov/350631/
  119. Tsui, J. H., Ostrovsky-Snider, N. A., Yama, D. M., Donohue, J. D., Choi, J. S., Chavanachat, R., Larson, J. D., Murphy, A. R., & Kim, D.-H. (2018). Conductive silk–polypyrrole composite scaffolds with bioinspired nanotopographic cues for cardiac tissue engineering. Journal of materials chemistry B, 6(44), 7185-7196. https://doi.org/10.1039/C8TB01116H
  120. Tufan, Y., Öztatlı, H., Doganay, D., Buyuksungur, A., Cicek, M. O., Döş, I. p. T. c. e., Berberoglu, C., Unalan, H. E., Garipcan, B., & Ercan, B. (2023). Multifunctional Silk Fibroin/Carbon Nanofiber Scaffolds for In Vitro Cardiomyogenic Differentiation of Induced Pluripotent Stem Cells and Energy Harvesting from Simulated Cardiac Motion. ACS Applied Materials & Interfaces, 15(36), 42271-42283. https://doi.org/10.1021/acsami.3c08601
  121. Wang, A., Liu, Z., Hu, M., Wang, C., Zhang, X., Shi, B., Fan, Y., Cui, Y., Li, Z., & Ren, K. (2018). Piezoelectric nanofibrous scaffolds as in vivo energy harvesters for modifying fibroblast alignment and proliferation in wound healing. Nano Energy, 43, 63-71. https://doi.org/10.1016/j.nanoen.2017.11.023
  122. Yamada, M., Tanemura, K., Okada, S., Iwanami, A., Nakamura, M., Mizuno, H., Ozawa, M., Ohyama-Goto, R., Kitamura, N., & Kawano, M. (2007). Electrical stimulation modulates fate determination of differentiating embryonic stem cells. Stem cells, 25(3), 562-570. https://doi.org/10.1634/stemcells.2006-0011
  123. You, J.-O., Rafat, M., Ye, G. J., & Auguste, D. T. (2011). Nanoengineering the heart: conductive scaffolds enhance connexin 43 expression. Nano letters, 11(9), 3643-3648. https://doi.org/10.1021/nl201514a
  124. Yucel, T., Cebe, P., & Kaplan, D. L. (2011). Structural origins of silk piezoelectricity. Advanced functional materials, 21(4), 779-785. https://doi.org/10.1002/adfm.201002077
  125. Zanjanizadeh Ezazi, N., Ajdary, R., Correia, A., Mäkilä, E., Salonen, J., Kemell, M., Hirvonen, J., Rojas, O. J., Ruskoaho, H. J., & Santos, H. l. A. (2020). Fabrication and characterization of drug-loaded conductive poly (glycerol sebacate)/nanoparticle-based composite patch for myocardial infarction applications. ACS applied materials & interfaces, 12(6), 6899-6909. https://doi.org/10.1021/acsami.9b21066
  126. Zaszczynska, A., Sajkiewicz, P., & Gradys, A. (2020). Piezoelectric Scaffolds as Smart Materials for Neural Tissue Engineering. Polymers (Basel), 12(1). https://doi.org/10.3390/polym12010161
  127. Zhang, X., Wang, T., Zhang, Z., Liu, H., Li, L., Wang, A., Ouyang, J., Xie, T., Zhang, L., Xue, J., & Tao, W. (2023b). Electrical stimulation system based on electroactive biomaterials for bone tissue engineering. Materials Today, 68, 177-203. https:/doi.org/10.1016/j.mattod.2023.06.011
  128. Zhao, G., Qing, H., Huang, G., Genin, G. M., Lu, T. J., Luo, Z., Xu, F., & Zhang, X. (2018). Reduced graphene oxide functionalized nanofibrous silk fibroin matrices for engineering excitable tissues. NPG Asia Materials, 10(10), 982-994. https://doi.org/10.1038/s41427-018-0092-8
  129. Zhao, G., Bao, X., Huang, G., Xu, F., & Zhang, X. (2019). Differential Effects of Directional Cyclic Stretching on the Functionalities of Engineered Cardiac Tissues. ACS Applied Bio Materials, 2(8), 3508-3519. https://doi.org/10.1021/acsabm.9b00414
  130. Zhou, X., Li, G., Wu, D., Liang, H., Zhang, W., Zeng, L., Zhu, Q., Lai, P., Wen, Z., & Yang, C. (2023a). Recent advances of cellular stimulation with triboelectric nanogenerators. Exploration, https://doi.org/10.1002/EXP.20220090
  131. Zhou, Y., Zhang, J. H., Li, S., Qiu, H., Shi, Y., & Pan, L. (2023b). Triboelectric Nanogenerators Based on 2D Materials: From Materials and Devices to Applications. Micromachines, 14(5), 1043. https://doi.org/10.3390/mi14051043
  132. Zhu, J., Peng, H., Rodriguez‐Macias, F., Margrave, J. L., Khabashesku, V. N., Imam, A. M., Lozano, K., & Barrera, E. V. (2004). Reinforcing epoxy polymer composites through covalent integration of functionalized nanotubes. Advanced Functional Materials, 14(7), 643-648. https://doi.org/10.1002/adfm.200305162
  133. Zhu, K., Shin, S. R., van Kempen, T., Li, Y. C., Ponraj, V., Nasajpour, A., Mandla, S., Hu, N., Liu, X., & Leijten, J. (2017). Gold nanocomposite bioink for printing 3D cardiac constructs. Advanced Functional Materials, 27(12), 1605352. https://doi.org/10.1002/adfm.201605352
Journal of Advanced Materials and Technologies
Volume 14, Issue 2
Summer 2025
Pages 1-25

  • Receive Date 16 February 2025
  • Revise Date 12 March 2025
  • Accept Date 01 June 2025