Vascular Remodeling of Clinically Used Patches and Decellularized Pericardial Matrices Recellularized with Autologous or Allogeneic Cells in a Porcine Carotid Artery Model

Chlupac, Jaroslav; Matejka, Roman; Konarik, Miroslav; Novotny, Robert; Simunkova, Zuzana; Mrazova, Iveta; Fabian, Ondrej; Zapletal, Milan; Pulda, Zdenek; Lipensky, Jan Falk; Stepanovska, Jana; Hanzalek, Karel; Broz, Antonin; Novak, Tomas; Lodererova, Alena; Voska, Ludek; Adla, Theodor; Fronek, Jiri; Rozkot, Miroslav; Forostyak, Serhiy; Kneppo, Peter; Bacakova, Lucie; Pirk, Jan

doi:10.3390/ijms23063310

Open AccessArticle

Vascular Remodeling of Clinically Used Patches and Decellularized Pericardial Matrices Recellularized with Autologous or Allogeneic Cells in a Porcine Carotid Artery Model

by

Jaroslav Chlupac

^1,2,3,*,†

,

Roman Matejka

^4,†

,

Miroslav Konarik

^5,6,

Robert Novotny

¹,

Zuzana Simunkova

⁷,

Iveta Mrazova

⁷,

Ondrej Fabian

⁸

,

Milan Zapletal

⁹,

Zdenek Pulda

⁹,

Jan Falk Lipensky

¹⁰,

Jana Stepanovska

⁴

,

Karel Hanzalek

⁴

,

Antonin Broz

²,

Tomas Novak

³,

Alena Lodererova

⁸,

Ludek Voska

⁸,

Theodor Adla

⁹,

Jiri Fronek

^1,3

,

Miroslav Rozkot

¹¹,

Serhiy Forostyak

¹⁰,

Peter Kneppo

⁴,

Lucie Bacakova

²

and

Jan Pirk

⁵ Show full author list Hide full author list

¹

Transplantation Surgery Department, Institute for Clinical and Experimental Medicine (IKEM), Videnska 1958/9, 14021 Prague, Czech Republic

²

Department of Biomaterials and Tissue Engineering, Institute of Physiology of the Czech Academy of Sciences, Videnska 1083, 14220 Prague, Czech Republic

³

Department of Anatomy, Second Faculty of Medicine, Charles University, V Uvalu 84, 15006 Prague, Czech Republic

⁴

Department of Biomedical Technology, Faculty of Biomedical Engineering, Czech Technical University in Prague, Nam. Sitna 3105, 27201 Kladno, Czech Republic

⁵

Cardiovascular Surgery Department, Institute for Clinical and Experimental Medicine (IKEM), Videnska 1958/9, 14021 Prague, Czech Republic

⁶

Institute of Physiology, First Faculty of Medicine, Charles University, Albertov 5, 12800 Prague, Czech Republic

⁷

Experimental Medicine Centre, Institute for Clinical and Experimental Medicine (IKEM), Videnska 1958/9, 14021 Prague, Czech Republic

⁸

Clinical and Transplant Pathology Centre, Institute for Clinical and Experimental Medicine (IKEM), Videnska 1958/9, 14021 Prague, Czech Republic

⁹

Radiodiagnostic and Interventional Radiology Department, Institute for Clinical and Experimental Medicine (IKEM), Videnska 1958/9, 14021 Prague, Czech Republic

¹⁰

PrimeCell Bioscience, a.s., Dr. Slabihoudka 6232/11, Poruba, 70800 Ostrava, Czech Republic

¹¹

Department of Pig Breeding, Institute of Animal Science, Komenskeho 1239, 51741 Kostelec nad Orlici, Czech Republic

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^*

Author to whom correspondence should be addressed.

^†

These authors contributed equally to this work.

Int. J. Mol. Sci. 2022, 23(6), 3310; https://doi.org/10.3390/ijms23063310

Submission received: 31 January 2022 / Revised: 4 March 2022 / Accepted: 12 March 2022 / Published: 18 March 2022

(This article belongs to the Special Issue Mechanisms of Cardiovascular Disease: Molecular Perspective)

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Abstract

Background: Cardiovascular surgery is confronted by a lack of suitable materials for patch repair. Acellular animal tissues serve as an abundant source of promising biomaterials. The aim of our study was to explore the bio-integration of decellularized or recellularized pericardial matrices in vivo. Methods: Porcine (allograft) and ovine (heterograft, xenograft) pericardia were decellularized using 1% sodium dodecyl sulfate ((1) Allo-decel and (2) Xeno-decel). We used two cell types for pressure-stimulated recellularization in a bioreactor: autologous adipose tissue-derived stromal cells (ASCs) isolated from subcutaneous fat of pigs ((3) Allo-ASC and (4) Xeno-ASC) and allogeneic Wharton’s jelly mesenchymal stem cells (WJCs) ((5) Allo-WJC and (6) Xeno-WJC). These six experimental patches were implanted in porcine carotid arteries for one month. For comparison, we also implanted six types of control patches, namely, arterial or venous autografts, expanded polytetrafluoroethylene (ePTFE Propaten^® Gore^®), polyethylene terephthalate (PET Vascutek^®), chemically stabilized bovine pericardium (XenoSure^®), and detoxified porcine pericardium (BioIntegral^® NoReact^®). The grafts were evaluated through the use of flowmetry, angiography, and histological examination. Results: All grafts were well-integrated and patent with no signs of thrombosis, stenosis, or aneurysm. A histological analysis revealed that the arterial autograft resembled a native artery. All other control and experimental patches developed neo-adventitial inflammation (NAI) and neo-intimal hyperplasia (NIH), and the endothelial lining was present. NAI and NIH were most prominent on XenoSure^® and Xeno-decel and least prominent on NoReact^®. In xenografts, the degree of NIH developed in the following order: Xeno-decel > Xeno-ASC > Xeno-WJC. NAI and patch resorption increased in Allo-ASC and Xeno-ASC and decreased in Allo-WJC and Xeno-WJC. Conclusions: In our setting, pre-implant seeding with ASC or WJC had a modest impact on vascular patch remodeling. However, ASC increased the neo-adventitial inflammatory reaction and patch resorption, suggesting accelerated remodeling. WJC mitigated this response, as well as neo-intimal hyperplasia on xenografts, suggesting immunomodulatory properties.

Keywords: blood vessel prosthesis; decellularization; cell seeding; tissue engineering; allograft; heterograft; pericardium; adipose tissue-derived stromal cells; Wharton’s jelly mesenchymal stem cells

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MDPI and ACS Style

Chlupac, J.; Matejka, R.; Konarik, M.; Novotny, R.; Simunkova, Z.; Mrazova, I.; Fabian, O.; Zapletal, M.; Pulda, Z.; Lipensky, J.F.; et al. Vascular Remodeling of Clinically Used Patches and Decellularized Pericardial Matrices Recellularized with Autologous or Allogeneic Cells in a Porcine Carotid Artery Model. Int. J. Mol. Sci. 2022, 23, 3310. https://doi.org/10.3390/ijms23063310

AMA Style

Chlupac J, Matejka R, Konarik M, Novotny R, Simunkova Z, Mrazova I, Fabian O, Zapletal M, Pulda Z, Lipensky JF, et al. Vascular Remodeling of Clinically Used Patches and Decellularized Pericardial Matrices Recellularized with Autologous or Allogeneic Cells in a Porcine Carotid Artery Model. International Journal of Molecular Sciences. 2022; 23(6):3310. https://doi.org/10.3390/ijms23063310

Chicago/Turabian Style

Chlupac, Jaroslav, Roman Matejka, Miroslav Konarik, Robert Novotny, Zuzana Simunkova, Iveta Mrazova, Ondrej Fabian, Milan Zapletal, Zdenek Pulda, Jan Falk Lipensky, and et al. 2022. "Vascular Remodeling of Clinically Used Patches and Decellularized Pericardial Matrices Recellularized with Autologous or Allogeneic Cells in a Porcine Carotid Artery Model" International Journal of Molecular Sciences 23, no. 6: 3310. https://doi.org/10.3390/ijms23063310

APA Style

Chlupac, J., Matejka, R., Konarik, M., Novotny, R., Simunkova, Z., Mrazova, I., Fabian, O., Zapletal, M., Pulda, Z., Lipensky, J. F., Stepanovska, J., Hanzalek, K., Broz, A., Novak, T., Lodererova, A., Voska, L., Adla, T., Fronek, J., Rozkot, M., ... Pirk, J. (2022). Vascular Remodeling of Clinically Used Patches and Decellularized Pericardial Matrices Recellularized with Autologous or Allogeneic Cells in a Porcine Carotid Artery Model. International Journal of Molecular Sciences, 23(6), 3310. https://doi.org/10.3390/ijms23063310

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Vascular Remodeling of Clinically Used Patches and Decellularized Pericardial Matrices Recellularized with Autologous or Allogeneic Cells in a Porcine Carotid Artery Model

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