Electroconductive cardiac patch based on bioactive PEDOT:PSS hydrogels.

PEDOT:PSS PVA cardiac patch conducting polymers hydrogel

Journal

Journal of biomedical materials research. Part A
ISSN: 1552-4965
Titre abrégé: J Biomed Mater Res A
Pays: United States
ID NLM: 101234237

Informations de publication

Date de publication:
30 Apr 2024
Historique:
revised: 13 04 2024
received: 26 12 2023
accepted: 22 04 2024
medline: 1 5 2024
pubmed: 1 5 2024
entrez: 1 5 2024
Statut: aheadofprint

Résumé

Engineering cardiac implants for treating myocardial infarction (MI) has advanced, but challenges persist in mimicking the structural properties and variability of cardiac tissues using traditional bioconstructs and conventional engineering methods. This study introduces a synthetic patch with a bioactive surface designed to swiftly restore functionality to the damaged myocardium. The patch combines a composite, soft, and conductive hydrogel-based on (3,4-ethylenedioxythiophene):polystyrene-sulfonate (PEDOT:PSS) and polyvinyl alcohol (PVA). This cardiac patch exhibits a reasonably high electrical conductivity (40 S/cm) and a stretchability up to 50% of its original length. Our findings reveal its resilience to 10% cyclic stretching at 1 Hz with no loss of conductivity over time. To mediate a strong cell-scaffold adhesion, we biofunctionalize the hydrogel with a N-cadherin mimic peptide, providing the cardiac patch with a bioactive surface. This modification promote increased adherence and proliferation of cardiac fibroblasts (CFbs) while effectively mitigating the formation of bacterial biofilm, particularly against Staphylococcus aureus, a common pathogen responsible for surgical site infections (SSIs). Our study demonstrates the successful development of a structurally validated cardiac patch possessing the desired mechanical, electrical, and biofunctional attributes for effective cardiac recovery. Consequently, this research holds significant promise in alleviating the burden imposed by myocardial infarctions.

Identifiants

pubmed: 38689450
doi: 10.1002/jbm.a.37729
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Fonds de recherche du Québec
ID : 174122
Organisme : Natural Sciences and Engineering Research Council of Canada (NSERC)
ID : RGPIN-2017-06319
Organisme : Natural Sciences and Engineering Research Council of Canada (NSERC)
ID : RGPIN-2020-05884

Informations de copyright

© 2024 The Authors. Journal of Biomedical Materials Research Part A published by Wiley Periodicals LLC.

Références

Benjamin EJ, Blaha MJ, Chiuve SE, et al. Heart disease and stroke Statistics‐2017 update: a report from the American Heart Association. Circulation. 2017;135(10):e146‐e603.
Bergmann O, Zdunek S, Felker A, et al. Dynamics of cell generation and turnover in the human heart. Cell. 2015;161(7):1566‐1575.
Kikuchi K, Poss KD. Cardiac regenerative capacity and mechanisms. Annu Rev Cell Dev Biol. 2012;28:719‐741.
Aliabadi A, Cochrane AB, Zuckermann AO. Current strategies and future trends in immunosuppression after heart transplantation. Curr Opin Organ Transplant. 2012;17(5):540‐545.
Li Y, Wei L, Lan L, et al. Conductive biomaterials for cardiac repair: a review. Acta Biomater. 2022;139:157‐178.
Mei X, Cheng K. Recent development in therapeutic cardiac patches. Front Cardiovasc Med. 2020;7:610364.
Mawad D, Mansfield C, Lauto A, et al. A conducting polymer with enhanced electronic stability applied in cardiac models. Sci Adv. 2016;2(11):e1601007.
Bahram M, Mohseni N, Moghtader M. An introduction to hydrogels and some recent applications. Emerging Concepts in Analysis and Applications of Hydrogels. IntechOpen; 2016.
Wang L, Liu Y, Ye G, et al. Injectable and conductive cardiac patches repair infarcted myocardium in rats and minipigs. Nat Biomed Eng. 2021;5(10):1157‐1173.
Liu K, Wei S, Song L, Liu H, Wang T. Conductive hydrogels—a novel material: recent advances and future perspectives. J Agric Food Chem. 2020;68(28):7269‐7280.
Stejskal J. Conducting polymer hydrogels. Chem Pap. 2017;71:269‐291.
Balint R, Cassidy NJ, Cartmell SH. Conductive polymers: towards a smart biomaterial for tissue engineering. Acta Biomater. 2014;10(6):2341‐2353.
Esmaeili H, Patino‐Guerrero A, Hasany M, et al. Electroconductive biomaterials for cardiac tissue engineering. Acta Biomater. 2022;139:118‐140.
Guimard NK, Gomez N, Schmidt CE. Conducting polymers in biomedical engineering. Prog Polym Sci. 2007;32(8–9):876‐921.
Fenoy GE, Azzaroni O, Knoll W, Marmisollé WA. Functionalization strategies of PEDOT and PEDOT: PSS films for organic bioelectronics applications. Chem. 2021;9(8):212.
Ul Haq A, Carotenuto F, De Matteis F, et al. Intrinsically conductive polymers for striated cardiac muscle repair. Int J Mol Sci. 2021;22(16):8550.
Groenendaal L, Jonas F, Freitag D, Pielartzik H, Reynolds JR. Poly (3, 4‐ethylenedioxythiophene) and its derivatives: past, present, and future. Adv Mater. 2000;12(7):481‐494.
Ghasemi‐Mobarakeh L, Prabhakaran MP, Morshed M, et al. Application of conductive polymers, scaffolds and electrical stimulation for nerve tissue engineering. J Tissue Eng Regen Med. 2011;5(4):e17‐e35.
Luo SC, Mohamed Ali E, Tansil NC, et al. Poly(3,4‐ethylenedioxythiophene) (PEDOT) nanobiointerfaces: thin, ultrasmooth, and functionalized PEDOT films with in vitro and in vivo biocompatibility. Langmuir. 2008;24(15):8071‐8077.
Karagkiozaki V, Karagiannidis PG, Gioti M, et al. Bioelectronics meets nanomedicine for cardiovascular implants: PEDOT‐based nanocoatings for tissue regeneration. Biochim Biophys Acta. 2013;1830(9):4294‐4304.
Bolin MH, Svennersten K, Wang X, et al. Nano‐fiber scaffold electrodes based on PEDOT for cell stimulation. Sens Actuators B. 2009;142(2):451‐456.
Asplund M, Thaning E, Lundberg J, et al. Toxicity evaluation of PEDOT/biomolecular composites intended for neural communication electrodes. Biomed Mater. 2009;4(4):045009.
Ning C, Zhou Z, Tan G, Zhu Y, Mao C. Electroactive polymers for tissue regeneration: developments and perspectives. Prog Polym Sci. 2018;81:144‐162.
Ravichandran R, Sundarrajan S, Venugopal JR, Mukherjee S, Ramakrishna S. Applications of conducting polymers and their issues in biomedical engineering. J R Soc Interface. 2010;7(suppl_5):S559‐S579.
Sun K, Zhang S, Li P, et al. Review on application of PEDOTs and PEDOT: PSS in energy conversion and storage devices. J Mater Sci Mater Electron. 2015;26:4438‐4462.
Rossetti N, Kateb P, Cicoira F. Neural and electromyography PEDOT electrodes for invasive stimulation and recording. J Mater Chem C. 2021;9(23):7243‐7263.
Abedi A, Hasanzadeh M, Tayebi L. Conductive nanofibrous Chitosan/PEDOT: PSS tissue engineering scaffolds. Mater Chem Phys. 2019;237:121882.
Zhou X, Kateb P, Fan J, et al. Conducting polymer films and bioelectrodes combining high adhesion and electro‐mechanical self‐healing. J Mater Chem C. 2024;12:5708‐5717.
Zhou X, Rajeev A, Subramanian A, et al. Self‐healing, stretchable, and highly adhesive hydrogels for epidermal patch electrodes. Acta Biomater. 2022;139:296‐306.
Kim C, Kateb P, Yeu J, et al. Flexible and stretchable printed conducting polymer devices for electrodermal activity measurements. Flexible Printed Electron. 2022;7(1):014008.
Petrossian G, Kateb P, Miquet‐Westphal F, Cicoira F. Advances in electrode materials for scalp, forehead, and ear EEG: a mini‐review. ACS Appl Bio Mater. 2023;6(8):3019‐3032.
Zhou X, Kateb P, Miquet‐Westphal F, Lodygensky GA, Cicoira F. Soft, conductive, and anti‐freezing conducting polymer organohydrogels. Adv Sens Res. 2023;2(12):2300072.
Kateb P, Fan J, Kim J, Zhou X, Lodygensky GA, Cicoira F. Printable, adhesive, and self‐healing dry epidermal electrodes based on PEDOT: PSS and polyurethane diol. Flexible Printed Electron. 2023;8(4):045006.
Hagler JE, Yeu J, Zhou X, Ducharme G, Amilhon B, Cicoira F. Electrodeposited PEDOT: BF4 coatings improve impedance of chronic neural stimulating probes in vivo. Adv Mater Interfaces. 2022;9(35):2201066.
Gong HY, Park J, Kim W, Kim J, Lee JY, Koh WG. A novel conductive and micropatterned PEG‐based hydrogel enabling the topographical and electrical stimulation of myoblasts. ACS Appl Mater Interfaces. 2019;11(51):47695‐47706.
Vara H, Collazos‐Castro JE. Biofunctionalized conducting polymer/carbon microfiber electrodes for ultrasensitive neural recordings. ACS Appl Mater Interfaces. 2015;7(48):27016‐27026.
Gupta S, Datt R, Mishra A, Tsoi WC, Patra A, Bober P. Poly (3, 4‐ethylenedioxythiophene): poly (styrene sulfonate) in antibacterial, tissue engineering and biosensors applications: Progress, challenges and perspectives. J Appl Polym Sci. 2022;139(30):e52663.
Ko Y, Kim J, Jeong HY, et al. Antibacterial poly (3,4‐ethylenedioxythiophene):poly(styrene‐sulfonate)/agarose nanocomposite hydrogels with thermo‐processability and self‐healing. Carbohydr Polym. 2019;203:26‐34.
Lu B, Yuk H, Lin S, et al. Pure PEDOT:PSS hydrogels. Nat Commun. 2019;10(1):1043.
Padavan DT, Hamilton AM, Millon LE, Boughner DR, Wan W. Synthesis, characterization and in vitro cell compatibility study of a poly(amic acid) graft/cross‐linked poly(vinyl alcohol) hydrogel. Acta Biomater. 2011;7(1):258‐267.
Raghavan K, Porterfield JE, Kottam AT, et al. Electrical conductivity and permittivity of murine myocardium. IEEE Trans Biomed Eng. 2009;56(8):2044‐2053.
Korn L, Lyra S, Ruschen D, Telyshev D, Leonhardt S, Walter M. In silico and in vitro conductivity models of the left heart ventricle. J Electr Bioimpedance. 2020;11(1):62‐71.
Stinstra JG, Hopenfeld B, MacLeod RS. On the passive cardiac conductivity. Ann Biomed Eng. 2005;33:1743‐1751.
Hassaballah AI, Hassan MA, Mardi AN, Hamdi M. An inverse finite element method for determining the tissue compressibility of human left ventricular wall during the cardiac cycle. PLoS One. 2013;8(12):e82703.
Nguyen‐Truong M, Li YV, Wang Z. Mechanical considerations of electrospun scaffolds for myocardial tissue and regenerative engineering. Bioengineering (Basel). 2020;7(4):122.
Silvestri A, Boffito M, Sartori S, Ciardelli G. Biomimetic materials and scaffolds for myocardial tissue regeneration. Macromol Biosci. 2013;13(8):984‐1019.
Iseri LT, Alexander LC, Mc CR, Boyle AJ, Myers GB. Water and electrolyte content of cardiac and skeletal muscle in heart failure and myocardial infarction. Am Heart J. 1952;43(2):215‐227.
Fallahi A, Mandla S, Kerr‐Phillip T, et al. Flexible and stretchable PEDOT‐embedded hybrid substrates for bioengineering and sensory applications. ChemNanoMat. 2019;5(6):729‐737.
Hoang A‐P, Ruprai H, Fidanovski K, et al. Porous and sutureless bioelectronic patch with retained electronic properties under cyclic stretching. Appl Mater Today. 2019;15:315‐322.
Zhang Y‐F, Guo M‐M, Zhang Y, et al. Flexible, stretchable and conductive PVA/PEDOT: PSS composite hydrogels prepared by SIPN strategy. Polym Test. 2020;81:106213.
Roshanbinfar K, Vogt L, Greber B, et al. Electroconductive biohybrid hydrogel for enhanced maturation and beating properties of engineered cardiac tissues. Adv Funct Mater. 2018;28(42):1803951.
Feig VR, Tran H, Lee M, Bao Z. Mechanically tunable conductive interpenetrating network hydrogels that mimic the elastic moduli of biological tissue. Nat Commun. 2018;9(1):2740.
Lari A, Sun T, Sultana N. PEDOT: PSS‐containing nanohydroxyapatite/chitosan conductive bionanocomposite scaffold: fabrication and evaluation. J Nanomater. 2016;2016:1‐12.
Hall C, Gehmlich K, Denning C, Pavlovic D. Complex relationship between cardiac fibroblasts and cardiomyocytes in health and disease. J Am Heart Assoc. 2021;10(5):e019338.
Loh CY, Chai JY, Tang TF, et al. The E‐cadherin and N‐cadherin switch in epithelial‐to‐mesenchymal transition: signaling, therapeutic implications, and challenges. Cells. 2019;8(10):1118.
Giamarellou H. Nosocomial cardiac infections. J Hosp Infect. 2002;50(2):91‐105.
Achinas S, Charalampogiannis N, Euverink GJW. A brief recap of microbial adhesion and biofilms. Appl Sci. 2019;9(14):2801.
Geng C, Fan L‐a, Niu H, et al. Improved anti‐organic fouling and antibacterial properties of PVDF ultrafiltration membrane by one‐step grafting imidazole‐functionalized graphene oxide. Mater Sci Eng C. 2021;131:112517.
Hu Y, Shen Y, Wu X, Tu X, Wang G‐X. Synthesis and biological evaluation of coumarin derivatives containing imidazole skeleton as potential antibacterial agents. Eur J Med Chem. 2018;143:958‐969.

Auteurs

Erwan Sauvage (E)

Department of Chemical Engineering, Polytechnique Montréal, Montréal, Quebec, Canada.

Justin Matta (J)

Department of Experimental Surgery, Faculty of Medicine, McGill University, Montreal, Quebec, Canada.

Cat-Thy Dang (CT)

Department of Chemical Engineering, Polytechnique Montréal, Montréal, Quebec, Canada.

Jiaxin Fan (J)

Department of Chemical Engineering, Polytechnique Montréal, Montréal, Quebec, Canada.

Graziele Cruzado (G)

Department of Chemical Engineering, Polytechnique Montréal, Montréal, Quebec, Canada.

Fabio Cicoira (F)

Department of Chemical Engineering, Polytechnique Montréal, Montréal, Quebec, Canada.

Géraldine Merle (G)

Department of Chemical Engineering, Polytechnique Montréal, Montréal, Quebec, Canada.

Classifications MeSH