Pericardium decellularization in a one-day, two-step protocol.
Decellularization
Human acellular matrix
Pericardial allograft
Tissue engineering
Tissue establishment
Journal
Molecular and cellular biochemistry
ISSN: 1573-4919
Titre abrégé: Mol Cell Biochem
Pays: Netherlands
ID NLM: 0364456
Informations de publication
Date de publication:
10 Sep 2024
10 Sep 2024
Historique:
received:
31
05
2023
accepted:
01
08
2024
medline:
10
9
2024
pubmed:
10
9
2024
entrez:
9
9
2024
Statut:
aheadofprint
Résumé
Scaffolds used in tissue engineering can be obtained from synthetic or natural materials, always focusing the effort on mimicking the extracellular matrix of human native tissue. In this study, a decellularization process is used to obtain an acellular, biocompatible non-cytotoxic human pericardium graft as a bio-substitute. An enzymatic and hypertonic method was used to decellularize the pericardium. Histological analyses were performed to determine the absence of cells and ensure the integrity of the extracellular matrix (ECM). In order to measure the effect of the decellularization process on the tissue's biological and mechanical properties, residual genetic content and ECM biomolecules (collagen, elastin, and glycosaminoglycan) were quantified and the tissue's tensile strength was tested. Preservation of the biomolecules, a residual genetic content below 50 ng/mg dry tissue, and maintenance of the histological structure provided evidence for the efficacy of the decellularization process, while preserving the ECM. Moreover, the acellular tissue retains its mechanical properties, as shown by the biomechanical tests. Our group has shown that the acellular pericardial matrix obtained through the super-fast decellularization protocol developed recently retains the desired biomechanical and structural properties, suggesting that it is suitable for a broad range of clinical indications.
Identifiants
pubmed: 39251464
doi: 10.1007/s11010-024-05086-x
pii: 10.1007/s11010-024-05086-x
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s).
Références
Castells-Sala C, Alemany-Ribes M, Fernández-Muiños T et al (2015) Current applications of tissue engineering in biomedicine. J Biochips Tissue Chips. https://doi.org/10.4172/2153-0777.s2-004
doi: 10.4172/2153-0777.s2-004
Inci I, Norouz Dizaji A, Ozel C et al (2020) Decellularized inner body membranes for tissue engineering: a review. J Biomater Sci Polym Ed 31:1287–1368. https://doi.org/10.1080/09205063.2020.1751523
doi: 10.1080/09205063.2020.1751523
pubmed: 32249722
Dutta RC, Dutta AK (2009) Cell-interactive 3D-scaffold; advances and applications. Biotechnol Adv 27:334–339. https://doi.org/10.1016/j.biotechadv.2009.02.002
doi: 10.1016/j.biotechadv.2009.02.002
pubmed: 19232387
Castells-sala C, Prat-vidal C, Roura S et al (2022) Human pericardial extracellular matrix : an implantation platform for cardiac tissue engineering. Front Biomater Sci. https://doi.org/10.3389/fbiom.2022.953837
doi: 10.3389/fbiom.2022.953837
Rodriguez ER, Tan CD (2017) Structure and anatomy of the human pericardium. Prog Cardiovasc Dis 59:327–340. https://doi.org/10.1016/j.pcad.2016.12.010
doi: 10.1016/j.pcad.2016.12.010
pubmed: 28062264
Ricci KB, Higgins R, Daniels VC, Kilic A (2014) Bovine pericardial reconstruction of the diaphragm after a heart transplant. Exp Clin Trans Off J Middle East Soc Organ Transplant 12:277–278
Yaliniz H, Salih OK, Atalay A et al (2014) Short-and mid-term results of xenograft–bovine pericardial patch in the repair of intracardiac defects: final results of a single-centre study. Cardiol Young 24:510–514
doi: 10.1017/S1047951113000711
pubmed: 23694855
Ascaso M, Pruna-Guillen R, Quintana E (2021) Postinfarction posterior ventricular septal defect repair: Infarct exclusion technique. Multimed Man Cardiothorac Surg. https://doi.org/10.1510/mmcts.2021.078
doi: 10.1510/mmcts.2021.078
pubmed: 34874626
Mihalj M, Pasic M, Carrel T (2022) The “beating-heart butterfly technique” for repair of basal post-infarction ventricle septum defect. Interact Cardiovasc Thorac Surg 34:919–920. https://doi.org/10.1093/icvts/ivac026
doi: 10.1093/icvts/ivac026
pubmed: 35134948
pmcid: 9070524
Grebenik EA, Gafarova ER, Istranov LP et al (2013) Mammalian pericardium-based bioprosthetic materials in xenotransplantation and tissue engineering. Proteomics. https://doi.org/10.1002/jssc.201200569
doi: 10.1002/jssc.201200569
pubmed: 23456920
Sun H, Wang H, Diao Y et al (2018) Large retrospective study of artificial dura substitute in patients with traumatic brain injury undergo decompressive craniectomy. Brain Behav 8:1–7. https://doi.org/10.1002/brb3.907
doi: 10.1002/brb3.907
Niegowski LJ, Bravetti GE, Gillmann K et al (2020) Pericardium patch graft (Tutoplast) for bleb repair and bleb remodelling after nonpenetrating filtering surgery: 6-month outcomes. J Glaucoma 29:347–350. https://doi.org/10.1097/IJG.0000000000001474
doi: 10.1097/IJG.0000000000001474
pubmed: 32097253
Ashena Z, Holmes C, Nanavaty MA (2021) Pericardium patch graft for severe corneal wound burn. J Curr Ophthalmol 33:342–344. https://doi.org/10.4103/joco.joco_195_20
doi: 10.4103/joco.joco_195_20
pubmed: 34765825
pmcid: 8579793
Chen F, Deng J, Luo L et al (2022) Crosslinked decellularized porcine pericardium as a substrate for conjunctival reconstruction. Stem Cells Int. https://doi.org/10.1155/2022/7571146
doi: 10.1155/2022/7571146
pubmed: 36618021
pmcid: 9812602
Hedergott A, Pink-Theofylaktopoulos U, Neugebauer A, Fricke J (2021) Tendon elongation with bovine pericardium in strabismus surgery—indications beyond Graves’ orbitopathy. Graefe’s Arch Clin Exp Ophthalmol 259:145–155. https://doi.org/10.1007/s00417-020-04939-7
doi: 10.1007/s00417-020-04939-7
Solakoğlu Ö, Ofluoğlu D, Schwarzenbach H et al (2022) A 3-year prospective randomized clinical trial of alveolar bone crest response and clinical parameters through 1, 2, and 3 years of clinical function of implants placed 4 months after alveolar ridge preservation using two different allogeneic bone-graftin. Int J Implant Dent. https://doi.org/10.1186/s40729-022-00402-w
doi: 10.1186/s40729-022-00402-w
pubmed: 35102440
pmcid: 8804085
de Dorlodot C, De Bie G, Deggouj N et al (2015) Are bovine pericardium underlay xenograft and butterfly inlay autograft efficient for transcanal tympanoplasty? Eur Arch Oto-Rhino-Laryngology 272:327–331. https://doi.org/10.1007/s00405-013-2855-8
doi: 10.1007/s00405-013-2855-8
Sainsbury E, do Amaral R, Blayney AW et al (2022) Tissue engineering and regenerative medicine strategies for the repair of tympanic membrane perforations. Biomater Biosyst 6:100046. https://doi.org/10.1016/j.bbiosy.2022.100046
doi: 10.1016/j.bbiosy.2022.100046
pubmed: 36824158
pmcid: 9934438
Remi E, Khelil N, Di I et al (2011) Pericardial processing: challenges, outcomes and future prospects. Biomaterials science and engineering. InTech, London, pp 437–456
Pérez ML, Castells-sala C, López-chicón P et al (2021) Fast protocol for the processing of split-thickness skin into decellularized human dermal matrix. Tissue Cell. https://doi.org/10.1016/j.tice.2021.101572
doi: 10.1016/j.tice.2021.101572
pubmed: 34119882
Nieto-Nicolau N, López-Chicón P, Fariñas O et al (2021) Effective decellularization of human nerve matrix for regenerative medicine with a novel protocol. Cell Tissue Res 384:167–177. https://doi.org/10.1007/s00441-020-03317-3
doi: 10.1007/s00441-020-03317-3
pubmed: 33471198
Crapo PM, Gilbert TW, Badylak SFSF (2011) An overview of tissue and whole organ decellularisation processes. Biomaterials 32:3233–3243. https://doi.org/10.1016/j.biomaterials.2011.01.057.An
doi: 10.1016/j.biomaterials.2011.01.057.An
pubmed: 21296410
pmcid: 3084613
Gilbert TW, Sellaro TL, Badylak SF (2006) Decellularization of tissues and organs. Biomaterials 27:3675–3683. https://doi.org/10.1016/j.biomaterials.2006.02.014
doi: 10.1016/j.biomaterials.2006.02.014
pubmed: 16519932
Holland JDR, Webster G, Rooney P et al (2021) Effects of chemical and radiation sterilisation on the biological and biomechanical properties of decellularised porcine peripheral nerves. Front Bioeng Biotechnol 9:660453
doi: 10.3389/fbioe.2021.660453
pubmed: 34150728
pmcid: 8209421
Dearth CL, Keane TJ, Carruthers CA et al (2016) The effect of terminal sterilization on the material properties and in vivo remodeling of a porcine dermal biologic scaffold. Acta Biomater 33:78–87
doi: 10.1016/j.actbio.2016.01.038
pubmed: 26826528
De Wit RJJ, Van Dis DJ, Bertrand ME et al (2023) Scaffold-based tissue engineering: supercritical carbon dioxide as an alternative method for decellularization and sterilization of dense materials. Acta Biomater 155:323–332
doi: 10.1016/j.actbio.2022.11.028
pubmed: 36423818
Hodde J, Hiles M (2002) Virus safety of a porcine-derived medical device: evaluation of a viral inactivation method. Biotechnol Bioeng 79:211–216
doi: 10.1002/bit.10281
pubmed: 12115437
Singh R, Singh D, Singh A (2016) Radiation sterilization of tissue allografts: a review. World J Radiol 8:355. https://doi.org/10.4329/wjr.v8.i4.355
doi: 10.4329/wjr.v8.i4.355
pubmed: 27158422
pmcid: 4840193
Prat-Vidal C, Rodríguez-Gómez L, Aylagas M et al (2020) First-in-human PeriCord cardiac bioimplant: scalability and GMP manufacturing of an allogeneic engineered tissue graft. EBioMedicine. https://doi.org/10.1016/j.ebiom.2020.102729
doi: 10.1016/j.ebiom.2020.102729
pubmed: 32304998
pmcid: 7163319
International Organization for Standardization (2009) ISO 10993–1: Biological evaluation of medical devices — Part 1: evaluation and testing within a risk management process. Int Stand. https://doi.org/10.1109/IEEESTD.2007.4288250
doi: 10.1109/IEEESTD.2007.4288250
Yu Y, Alkhawaji A, Ding Y, Mei J (2016) Decellularized scaffolds in regenerative medicine. Oncotarget 7:58671–58683. https://doi.org/10.18632/oncotarget.10945
doi: 10.18632/oncotarget.10945
pubmed: 27486772
pmcid: 5295461
Terlecki P, Zubilewicz T, Wojtak A et al (2019) Replacement of infected aortoiliac vascular grafts with bifurcated biointegral surgical No-React® bovine pericardial xenografts. Xenotransplantation 26:e12496
doi: 10.1111/xen.12496
pubmed: 30767329
Anson JA, Marchand EP (1996) Bovine pericardium for dural grafts: clinical results in 35 patients. Neurosurgery 39:764–768
doi: 10.1097/00006123-199610000-00025
pubmed: 8880771
Edwards Lifescience Corporation (2022) Duravess bovine pericardial vascular patch. https://www.edwards.com/healthcare-professionals/products-services/vascular-solutions/duravess . Accessed 28 Nov 2022
HealthManagement.org Pericardial patch / bovine XenoSure®, Le Maitre Vascular. In: 2022. https://healthmanagement.org/products/view/pericardial-patch-bovine-xenosure-r-lemaitre-vascular . Accessed 28 Nov 2022
HealthManagement.org Pericardial patch / bovine SJM
Gurrado A, Franco IF, Lissidini G et al (2015) Impact of pericardium bovine patch (Tutomesh®) on incisional hernia treatment in contaminated or potentially contaminated fields: retrospective comparative study. Hernia 19:259–266
doi: 10.1007/s10029-014-1228-6
pubmed: 24584456
Bhatt H, Okafor L, Bhatt R (2022) Allogenic dehydrated human pericardium patch graft (Tutoplast): a novel use for reconstruction in orbital implant exposure. Eur J Ophthalmol 32:725–728
doi: 10.1177/11206721211004398
pubmed: 33736492
Wollmann L, Suss P, Mendonça J et al (2019) Characterization of decellularized human pericardium for tissue engineering and regenerative medicine applications. Arq Bras Cardiol 113:11–17
pubmed: 31271596
pmcid: 6684174
Musilkova J, Filova E, Pala J et al (2020) Human decellularized and crosslinked pericardium coated with bioactive molecular assemblies. Biomed Mater. https://doi.org/10.1088/1748-605X/ab52db
doi: 10.1088/1748-605X/ab52db
Montagner G, Barbazza A, Lugas AT et al (2023) Decellularized cryopreserved human pericardium: a validation study towards tissue bank practice. Cell Tissue Bank. https://doi.org/10.1007/s10561-023-10072-6
doi: 10.1007/s10561-023-10072-6
pubmed: 37728671
pmcid: 11142958
Gilpin A, Yang Y (2017) Decellularization strategies for regenerative medicine: from processing techniques to applications. Biomed Res Int 2017:1–13. https://doi.org/10.1155/2017/9831534
doi: 10.1155/2017/9831534
Le Maitre CardioCel® Bioscaffold. In: 2022. https://www.lemaitre.com/products/cardiocel-bioscaffold . Accessed 5 Dec 2022
Oswal D, Korossis S, Mirsadraee S et al (2007) Biomechanical characterization of decellularized and cross-linked bovine pericardium. J Heart Valve Dis 16:165
pubmed: 17484467
Jalili-Firoozinezhad S, Rajabi-Zeleti S, Marsano A et al (2016) Influence of decellularized pericardium matrix on the behavior of cardiac progenitors. J Appl Polym Sci. https://doi.org/10.1002/app.43255
doi: 10.1002/app.43255
Mirsadraee S, Wilcox HE, Korossis SA et al (2006) Development and characterization of an acellular human pericardial matrix for tissue engineering. Tissue Eng 12:763–773
doi: 10.1089/ten.2006.12.763
pubmed: 16674290
Vinci MC, Tessitore G, Castiglioni L et al (2013) Mechanical compliance and immunological compatibility of fixative-free decellularized/cryopreserved human pericardium. PLoS ONE 8:e64769
doi: 10.1371/journal.pone.0064769
pubmed: 23705010
pmcid: 3660606
Hussain SH, Limthongkul B, Humphreys TR (2013) The biomechanical properties of the skin. Dermatologic Surg 39:193–203. https://doi.org/10.1111/dsu.12095
doi: 10.1111/dsu.12095
Mendoza-Novelo B, Avila EE, Cauich-Rodríguez JV et al (2011) Decellularization of pericardial tissue and its impact on tensile viscoelasticity and glycosaminoglycan content. Acta Biomater 7:1241–1248. https://doi.org/10.1016/j.actbio.2010.11.017
doi: 10.1016/j.actbio.2010.11.017
pubmed: 21094703
de Lima EO, Ferrasi AC, Kaasi A (2019) Decellularization of human pericardium with potential application in regenerative medicine. Arq Bras Cardiol 113:18–19. https://doi.org/10.5935/abc.20190130
doi: 10.5935/abc.20190130
pubmed: 31411289
pmcid: 6684195
Putame G, Gabetti S, Carbonaro D et al (2020) Compact and tunable stretch bioreactor advancing tissue engineering implementation. application to engineered cardiac constructs. Med Eng Phys 84:1–9
doi: 10.1016/j.medengphy.2020.07.018
pubmed: 32977905
Belviso I, Romano V, Sacco AM et al (2020) Decellularized human dermal matrix as a biological scaffold for cardiac repair and regeneration. Front Bioeng Biotechnol 8:229
doi: 10.3389/fbioe.2020.00229
pubmed: 32266249
pmcid: 7099865
Carbonaro D, Putame G, Castaldo C et al (2020) A low-cost scalable 3D-printed sample-holder for agitation-based decellularization of biological tissues. Med Eng Phys 85:7–15
doi: 10.1016/j.medengphy.2020.09.006
pubmed: 33081966