In vitro and in vivo evaluation of biohybrid tissue-engineered vascular grafts with transformative 1H/19F MRI traceable scaffolds

Elena Rama; Saurav Ranjan Mohapatra; Yukiharu Sugimura; Tomoyuki Suzuki; Stefan Siebert; Roman Barmin; Juliane Hermann; Jasmin Baier; Anne Rix; Teresa Lemainque; Susanne Koletnik; Asmaa Said Elshafei; Roger Molto Pallares; Seyed Mohammadali Dadfar; René H Tolba; Volkmar Schulz; Joachim Jankowski; Christian Apel; Payam Akhyari; Stefan Jockenhoevel; Fabian Kiessling

doi:10.1016/j.biomaterials.2024.122669

In vitro and in vivo evaluation of biohybrid tissue-engineered vascular grafts with transformative ¹H/¹⁹F MRI traceable scaffolds

Biomaterials. 2024 Jun 17:311:122669. doi: 10.1016/j.biomaterials.2024.122669. Online ahead of print.

Authors

Elena Rama¹, Saurav Ranjan Mohapatra², Yukiharu Sugimura³, Tomoyuki Suzuki³, Stefan Siebert², Roman Barmin¹, Juliane Hermann⁴, Jasmin Baier¹, Anne Rix¹, Teresa Lemainque⁵, Susanne Koletnik¹, Asmaa Said Elshafei¹, Roger Molto Pallares¹, Seyed Mohammadali Dadfar⁶, René H Tolba⁷, Volkmar Schulz¹, Joachim Jankowski⁸, Christian Apel², Payam Akhyari³, Stefan Jockenhoevel², Fabian Kiessling⁹

Affiliations

¹ Institute for Experimental Molecular Imaging, Faculty of Medicine, RWTH Aachen University, Forckenbeckstraße 55, 52074 Aachen, Germany.
² Department of Biohybrid & Medical Textiles, AME-Institute of Applied Medical Engineering, Helmholtz Institute, RWTH Aachen University, Forckenbeckstraße 55, 52074 Aachen, Germany.
³ Department of Cardiac Surgery, Medical Faculty and RWTH University Hospital Aachen, RWTH Aachen University, Aachen, Germany.
⁴ Institute for Molecular Cardiovascular Research (IMCAR), University Hospital RWTH Aachen, Aachen, Germany.
⁵ Institute for Experimental Molecular Imaging, Faculty of Medicine, RWTH Aachen University, Forckenbeckstraße 55, 52074 Aachen, Germany; Department of Diagnostic and Interventional Radiology, Medical Faculty, RWTH Aachen University, 52074 Aachen, Germany.
⁶ Institute for Experimental Molecular Imaging, Faculty of Medicine, RWTH Aachen University, Forckenbeckstraße 55, 52074 Aachen, Germany; Ardena Oss, 5349 AB Oss, the Netherlands.
⁷ Institute for Laboratory Animal Science and Experimental Surgery, Medical Faculty, RWTH Aachen International University, Aachen, Germany.
⁸ Institute for Molecular Cardiovascular Research (IMCAR), University Hospital RWTH Aachen, Aachen, Germany; Aachen-Maastricht Institute for CardioRenal Disease (AMICARE), University Hospital RWTH Aachen, Aachen, Germany; Department of Pathology, Cardiovascular Research Institute Maastricht (CARIM), University of Maastricht, the Netherlands.
⁹ Institute for Experimental Molecular Imaging, Faculty of Medicine, RWTH Aachen University, Forckenbeckstraße 55, 52074 Aachen, Germany. Electronic address: fkiessling@ukaachen.de.

PMID: 38906013
DOI: 10.1016/j.biomaterials.2024.122669

Abstract

Biohybrid tissue-engineered vascular grafts (TEVGs) promise long-term durability due to their ability to adapt to hosts' needs. However, the latter calls for sensitive non-invasive imaging approaches to longitudinally monitor their functionality, integrity, and positioning. Here, we present an imaging approach comprising the labeling of non-degradable and degradable TEVGs' components for their in vitro and in vivo monitoring by hybrid ¹H/¹⁹F MRI. TEVGs (inner diameter 1.5 mm) consisted of biodegradable poly(lactic-co-glycolic acid) (PLGA) fibers passively incorporating superparamagnetic iron oxide nanoparticles (SPIONs), non-degradable polyvinylidene fluoride scaffolds labeled with highly fluorinated thermoplastic polyurethane (¹⁹F-TPU) fibers, a smooth muscle cells containing fibrin blend, and endothelial cells. ¹H/¹⁹F MRI of TEVGs in bioreactors, and after subcutaneous and infrarenal implantation in rats, revealed that PLGA degradation could be faithfully monitored by the decreasing SPIONs signal. The ¹⁹F signal of ¹⁹F-TPU remained constant over weeks. PLGA degradation was compensated by cells' collagen and α-smooth-muscle-actin deposition. Interestingly, only TEVGs implanted on the abdominal aorta contained elastin. XTT and histology proved that our imaging markers did not influence extracellular matrix deposition and host immune reaction. This concept of non-invasive longitudinal assessment of cardiovascular implants using ¹H/¹⁹F MRI might be applicable to various biohybrid tissue-engineered implants, facilitating their clinical translation.

Keywords: (19)F-TPU; Hybrid (1)H/(19)F MRI; Molecular imaging; PLGA; SPIONs; Tissue-engineering.