In Situ Remodeling Overrules Bioinspired Scaffold Architecture of Supramolecular Elastomeric Tissue-Engineered Heart Valves

Overview

Journal JACC Basic Transl Sci

Date 2021 Jan 11

PMID 33426376

Citations 27

Authors

Marcelle Uiterwijk

Anthal I P M Smits

Daphne van Geemen

Bas van Klarenbosch

Sylvia Dekker

Maarten Jan Cramer

Jan Willem van Rijswijk

Emily B Lurier

Andrea Di Luca

Marieke C P Brugmans

Tristan Mes

Anton W Bosman

Elena Aikawa

Paul F Grundeman

Carlijn V C Bouten

Jolanda Kluin

Affiliations

Soon will be listed here.

Abstract

In situ tissue engineering that uses resorbable synthetic heart valve scaffolds is an affordable and practical approach for heart valve replacement; therefore, it is attractive for clinical use. This study showed no consistent collagen organization in the predefined direction of electrospun scaffolds made from a resorbable supramolecular elastomer with random or circumferentially aligned fibers, after 12 months of implantation in sheep. These unexpected findings and the observed intervalvular variability highlight the need for a mechanistic understanding of the long-term in situ remodeling processes in large animal models to improve predictability of outcome toward robust and safe clinical application.

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References

Serrani M, Brubert J, Stasiak J, De Gaetano F, Zaffora A, Costantino M . A Computational Tool for the Microstructure Optimization of a Polymeric Heart Valve Prosthesis. J Biomech Eng. 2016; 138(6):061001. PMC: 4866470. DOI: 10.1115/1.4033178. View

van Hout G, Teuben M, Heeres M, de Maat S, De Jong R, Maas C . Invasive surgery reduces infarct size and preserves cardiac function in a porcine model of myocardial infarction. J Cell Mol Med. 2015; 19(11):2655-63. PMC: 4627570. DOI: 10.1111/jcmm.12656. View

Neumann A, Sarikouch S, Breymann T, Cebotari S, Boethig D, Horke A . Early systemic cellular immune response in children and young adults receiving decellularized fresh allografts for pulmonary valve replacement. Tissue Eng Part A. 2013; 20(5-6):1003-11. PMC: 3938920. DOI: 10.1089/ten.TEA.2013.0316. View

Kluin J, Talacua H, Smits A, Emmert M, Brugmans M, Fioretta E . In situ heart valve tissue engineering using a bioresorbable elastomeric implant - From material design to 12 months follow-up in sheep. Biomaterials. 2017; 125:101-117. DOI: 10.1016/j.biomaterials.2017.02.007. View

Krynauw H, Buescher J, Koehne J, Verrijt L, Limbert G, Davies N . Tissue Ingrowth Markedly Reduces Mechanical Anisotropy and Stiffness in Fibre Direction of Highly Aligned Electrospun Polyurethane Scaffolds. Cardiovasc Eng Technol. 2020; 11(4):456-468. DOI: 10.1007/s13239-020-00475-x. View

van Haaften E, Wissing T, Kurniawan N, Smits A, Bouten C . Human In Vitro Model Mimicking Material-Driven Vascular Regeneration Reveals How Cyclic Stretch and Shear Stress Differentially Modulate Inflammation and Matrix Deposition. Adv Biosyst. 2020; 4(6):e1900249. DOI: 10.1002/adbi.201900249. View

Syedain Z, Reimer J, Schmidt J, Lahti M, Berry J, Bianco R . 6-month aortic valve implantation of an off-the-shelf tissue-engineered valve in sheep. Biomaterials. 2015; 73:175-84. PMC: 5520964. DOI: 10.1016/j.biomaterials.2015.09.016. View

Driessen-Mol A, Emmert M, Dijkman P, Frese L, Sanders B, Weber B . Transcatheter implantation of homologous "off-the-shelf" tissue-engineered heart valves with self-repair capacity: long-term functionality and rapid in vivo remodeling in sheep. J Am Coll Cardiol. 2013; 63(13):1320-1329. DOI: 10.1016/j.jacc.2013.09.082. View

Ayoub S, Ferrari G, Gorman R, Gorman J, Schoen F, Sacks M . Heart Valve Biomechanics and Underlying Mechanobiology. Compr Physiol. 2016; 6(4):1743-1780. PMC: 5537387. DOI: 10.1002/cphy.c150048. View

10.

Chester A, El-Hamamsy I, Butcher J, Latif N, Bertazzo S, Yacoub M . The living aortic valve: From molecules to function. Glob Cardiol Sci Pract. 2014; 2014(1):52-77. PMC: 4104380. DOI: 10.5339/gcsp.2014.11. View

11.

Battiston K, Labow R, Simmons C, Santerre J . Immunomodulatory polymeric scaffold enhances extracellular matrix production in cell co-cultures under dynamic mechanical stimulation. Acta Biomater. 2015; 24:74-86. DOI: 10.1016/j.actbio.2015.05.038. View

12.

Wagenseil J, Mecham R . New insights into elastic fiber assembly. Birth Defects Res C Embryo Today. 2008; 81(4):229-40. DOI: 10.1002/bdrc.20111. View

13.

Li Q, Bai Y, Jin T, Wang S, Cui W, Stanciulescu I . Bioinspired Engineering of Poly(ethylene glycol) Hydrogels and Natural Protein Fibers for Layered Heart Valve Constructs. ACS Appl Mater Interfaces. 2017; 9(19):16524-16535. DOI: 10.1021/acsami.7b03281. View

14.

Motta S, Lintas V, Fioretta E, Dijkman P, Putti M, Caliskan E . Human cell-derived tissue-engineered heart valve with integrated Valsalva sinuses: towards native-like transcatheter pulmonary valve replacements. NPJ Regen Med. 2019; 4:14. PMC: 6572861. DOI: 10.1038/s41536-019-0077-4. View

15.

Wissing T, van Haaften E, Koch S, Ippel B, Kurniawan N, Bouten C . Hemodynamic loads distinctively impact the secretory profile of biomaterial-activated macrophages - implications for in situ vascular tissue engineering. Biomater Sci. 2019; 8(1):132-147. DOI: 10.1039/c9bm01005j. View

16.

Dekker S, van Geemen D, van den Bogaerdt A, Driessen-Mol A, Aikawa E, Smits A . Sheep-Specific Immunohistochemical Panel for the Evaluation of Regenerative and Inflammatory Processes in Tissue-Engineered Heart Valves. Front Cardiovasc Med. 2018; 5:105. PMC: 6104173. DOI: 10.3389/fcvm.2018.00105. View

17.

Moreira R, Neusser C, Kruse M, Mulderrig S, Wolf F, Spillner J . Tissue-Engineered Fibrin-Based Heart Valve with Bio-Inspired Textile Reinforcement. Adv Healthc Mater. 2016; 5(16):2113-21. DOI: 10.1002/adhm.201600300. View

18.

Mela P . Subject- and Leaflet-Specific Remodeling of Polymeric Heart Valves for In Situ Tissue Engineering: Challenges Towards Clinical Translation. JACC Basic Transl Sci. 2020; 5(1):32-34. PMC: 7000880. DOI: 10.1016/j.jacbts.2019.12.006. View

19.

Loerakker S, Argento G, Oomens C, Baaijens F . Effects of valve geometry and tissue anisotropy on the radial stretch and coaptation area of tissue-engineered heart valves. J Biomech. 2013; 46(11):1792-800. DOI: 10.1016/j.jbiomech.2013.05.015. View

20.

Tseng H, Puperi D, Kim E, Ayoub S, Shah J, Cuchiara M . Anisotropic poly(ethylene glycol)/polycaprolactone hydrogel-fiber composites for heart valve tissue engineering. Tissue Eng Part A. 2014; 20(19-20):2634-45. PMC: 4195534. DOI: 10.1089/ten.TEA.2013.0397. View