Tissue-specific extracellular matrix promotes tissue regeneration and repair. We aimed to identify the optimal decellularized matrices for tissue-engineered vascular graft (TEVG).
Methods:
Decellularized aorta of fetal pigs (DAFP, n = 6, group A), decellularized aorta of adult pigs (DAAP, n = 6, group B), and decellularized carotid artery of adult pigs (DCAP, n = 6, group C) were prepared. Scaffolds were compared using histology and ultrastructure. Endothelial cell (EC) and myofibroblast (MFB) infiltration assessments were performed in vitro. Cell infiltration was measured in vivo. Biomechanical properties were also determined.
Results:
Almost original cells were removed by the acellularization procedure, while the construction of the matrix basically remained. In vitro, monolayer ECs and multi-layer MFBs were formed onto the internal surface of the specimens after 3 weeks. In vivo, cell infiltration in group A significantly increased at the 6th and 8th week when compared with groups B and C (p < 0.01). The infiltrated cells were mainly MFBs and a few CD4+ T-lymphocytes/macrophages in the specimens. Groups A and B showed greater axial compliance than group C (p < 0.01).
Conclusion:
DAFP was the most suitable for use as a small-caliber vascular graft.
CriquiMHAboyansV.Epidemiology of peripheral artery disease. Circ Res2015; 116(9): 1509–1526.
4.
MozaffarianDBenjaminEJGoAS, et al. Executive summary: heart disease and stroke statistics—2016 update: a report from the American Heart Association. Circulation2016; 133(4): 447–454.
HuangAHNiklasonLE.Engineering of arteries in vitro. Cell Mol Life Sci2014; 71(11): 2103–2118.
7.
CarrabbaMMadedduP.Current strategies for the manufacture of small size tissue engineering vascular grafts. Front Bioeng Biotechnol2018; 6: 41.
8.
NegishiJHashimotoYYamashitaA, et al. Evaluation of small-diameter vascular grafts reconstructed from decellularized aorta sheets. J Biomed Mater Res A2017; 105(5): 1293–1298.
9.
HasanAMemicAAnnabiN, et al. Electrospun scaffolds for tissue engineering of vascular grafts. Acta Biomater2014; 10(1): 11–25.
10.
PunnakitikashemPTruongDMenonJU, et al. Electrospun biodegradable elastic polyurethane scaffolds with dipyridamole release for small diameter vascular grafts. Acta Biomater2014; 10(11): 4618–4628.
11.
XieYGuanYKimSH, et al. The mechanical performance of weft-knitted/electrospun bilayer small diameter vascular prostheses. J Mech Behav Biomed Mater2016; 61: 410–418.
12.
ThomasAperMathias, et al. Novel method for the generation of tissue-engineered vascular grafts based on a highly compacted fibrin matrix. Acta Biomater2016; 29: 21–32.
13.
ZhangYLiXSGuexAG, et al. A compliant and biomimetic three-layered vascular graft for small blood vessels. Biofabrication2017; 9(2): 025010.
14.
ZhangFXieYCelikH, et al. Engineering small-caliber vascular grafts from collagen filaments and nanofibers with comparable mechanical properties to native vessels. Biofabrication2019; 11(3): 035020.
15.
DevineCHonsBMccollumC.Heparin-bonded dacron or polytetrafluoroethylene for femoropopliteal bypass grafting: a multicenter trial. J Vasc Surg2001; 33(3): 533–539.
16.
TschoekeBFlanaganTCKochS, et al. Tissue-engineered small-caliber vascular graft based on a novel biodegradable composite fibrin-polylactide scaffold. Tissue Eng A2009; 15(8): 1909–1918.
17.
HamaguchiMOkudaYKatamiK, et al. Short-term thrombogenicity and patency of expanded polytetrafluoroethylene (ePTFE) vascular grafts with varying wall structure. J Jpn Socr Artif Organs Tissues1994; 23: 832–837.
18.
MirsadraeeSWilcoxHEKorossisSA, et al. Development and characterization of an acellular human pericardial matrix for tissue engineering. Tissue Eng2006; 12(4): 763–773.
19.
RoySSilacciPStergiopulosN.Biomechanical properties of decellularized porcine common carotid arteries. Am J Physiol Heart Circ Physiol2005; 289(4): H1567–H1576.
20.
GrabowNSchmohlKKhosraviA, et al. Mechanical and structural properties of a novel hybrid heart valve scaffold for tissue engineering. Artif Organs2004; 28(11): 971–979.
21.
KorossisSAWilcoxHEWattersonKG, et al. In-vitro assessment of the functional performance of the decellularized intact porcine aortic root. J Heart Valve Dis2005; 14(3): 408–421.
22.
LiuRHOngCSFukunishiT, et al. Review of vascular graft studies in large animal models. Tissue Eng Part B Rev2018; 24(2): 133–143.
23.
XuSLuFChengL, et al. Preparation and characterization of small-diameter decellularized scaffolds for vascular tissue engineering in an animal model. Biomed Eng Online2017; 16(1): 55.
24.
ChoiHJLeeJJKimMK, et al. Cross-reactivity between decellularized porcine corneal lamellae for corneal xenobridging and subsequent corneal allotransplants. Xenotransplantation2014; 21(2): 115–123.
25.
MoroniFMirabellaT.Decellularized matrices for cardiovascular tissue engineering. Am J Stem Cells2014; 3(1): 1–20.
26.
WuPKimuraTTadokoroH, et al. Relation between the tissue structure and protein permeability of decellularized porcine aorta. Mater Sci Eng C2014; 43: 465–471.
27.
RowSSantandreuASwartzDD, et al. Cell-free vascular grafts: recent developments and clinical potential. Technology2017; 5(1): 13–20.
28.
CaiZGuYChengJ, et al. Decellularization, cross-linking and heparin immobilization of porcine carotid arteries for tissue engineering vascular grafts. Cell Tissue Bank2019; 20(4): 569–578.
29.
MaXHeZLiL, et al. Development and in vivo validation of tissue-engineered, small-diameter vascular grafts from decellularized aortae of fetal pigs and canine vascular endothelial cells. J Cardiothorac Surg2017; 12(1): 101.
30.
LiQHuangCXuZ, et al. The fetal porcine aorta and mesenteric acellular matrix as small-caliber tissue engineering vessels and microvasculature scaffold. Aesthetic Plast Surg2013; 37(4): 822–832.
31.
GalloMNasoFPoserH, et al. Physiological performance of a detergent decellularized heart valve implanted for 15 months in Vietnamese pigs: surgical procedure, follow-up, and explant inspection. Artif Organs2012; 36(6): E138–E150.
32.
LiuXCaiYXiaC, et al. An innovative method to obtain porous porcine aorta scaffolds for tissue engineering. Artif Organs2019; 43(12): 1162–1169.
33.
ChengJWangCGuY.Combination of freeze-thaw with detergents: a promising approach to the decellularization of porcine carotid arteries. Biomed Mater Eng2019; 30(2): 191–205.
34.
LiuG-FHeZ-JYangD-P, et al. Decellularized aorta of fetal pigs as a potential scaffold for small diameter tissue engineered vascular graft. Chin Med J2008; 121(15): 1398–1406.
35.
MallJWPhilippAWRademacherA, et al. Re-endothelialization of punctured ePTFE graft: an in vitro study under pulsed perfusion conditions. Nephrol Dial Transplant2004; 19(1): 61–67.
36.
DahlSLRhimCSongYC, et al. Mechanical properties and compositions of tissue engineered and native arteries. Ann Biomed Eng2007; 35(3): 348–355.
37.
KasimirMTRiederESeebacherG, et al. Comparison of different decellularization procedures of porcine heart valves. Int J Artif Organs2003; 26(5): 421–427.
38.
HoshibaTLuHKawazoeN, et al. Decellularized matrices for tissue engineering. Expert Opin Biol Ther2010; 10(12): 1717–1728.
39.
SchmidtCEBaierJM.Acellular vascular tissues: natural biomaterials for tissue repair and tissue engineering. Biomaterials2000; 21(22): 2215–2231.
40.
LinC-HHsiaKMaH, et al. In vivo performance of decellularized vascular grafts: a review article. Int J Mol Sci2018; 19(7): 2101.
41.
TaylorDASampaioLCFerdousZ, et al. Decellularized matrices in regenerative medicine. Acta Biomater2018; 74: 74–89.
42.
WangZMithieuxSMWeissAS.Fabrication techniques for vascular and vascularized tissue engineering. Adv Healthc Mater2019; 8(19): 1900742.
43.
PeterMCrapo, et al. An overview of tissue and whole organ decellularization processes. Biomaterials2011; 32(12): 3222–3243.
44.
SteinhoffGStockUKarimN, et al. Tissue engineering of pulmonary heart valves on allogenic acellular matrix conduits: in vivo restoration of valve tissue. Circulation2000; 102(19): III50–III55.
45.
SilvaARodriguesSCaldeiraJ, et al. Three-dimensional scaffolds of fetal decellularized hearts exhibit enhanced potential to support cardiac cells in comparison to the adult. Biomaterials2016; 104: 52–64.
46.
DidangelosAYinXMandalK, et al. Proteomics characterization of extracellular space components in the human aorta. Mol Cell Proteomics2010; 9(9): 2048–2062.
47.
SumbriaREndotheliumFM.Primer on cerebrovascular diseases. Amsterdam: Elsevier, 2017, pp. 47–51.
48.
SepúlvedaCPalomoIFuentesE.Mechanisms of endothelial dysfunction during aging: predisposition to thrombosis. Mech Ageing Dev2017; 164: 91–99.
49.
MogaldeaAHilfikerASchillingT, et al. Tissue engineering of regenerative cardiovascular patch material based on decellularized pericardium. Thorac Cardiovasc Surg2014; 62(S 01): SC2.
50.
BrennanJAArrizabalagaJHNollertMU.Development of a small diameter vascular graft using the human amniotic membrane. Cardiovasc Eng Technol2014; 5(1): 96–109.
51.
CoccioloneAJHawesJZCatalinSM, et al. Elastin, arterial mechanics, and cardiovascular disease. Am J Physiol Heart Circ Physiol2018; 315(2): H189–H205.
52.
KumarVACavesJMHallerCA, et al. Acellular vascular grafts generated from collagen and elastin analogues. Acta Biomater2013; 9(9): 8067–8074.
53.
MuraseYNaritaYKagamiH, et al. Evaluation of compliance and stiffness of decellularized tissues as scaffolds for tissue-engineered small caliber vascular grafts using intravascular ultrasound. ASAIO J2006; 52(4): 450–455.
54.
KarimiAMilewiczDM.Structure of the elastin-contractile units in the thoracic aorta and how genes that cause thoracic aortic aneurysms and dissections disrupt this structure. Can J Cardiol2016; 32(1): 26–34.
55.
BrownBNLondonoRTotteyS, et al. Macrophage phenotype as a predictor of constructive remodeling following the implantation of biologically derived surgical mesh materials. Acta Biomater2012; 8(3): 978–987.
56.
BöerUHurtado-AguilarLGKlingenbergM, et al. Effect of intensified decellularization of equine carotid arteries on scaffold biomechanics and cytotoxicity. Ann Biomed Eng2015; 49(6): 748–748.
57.
OwensEAJieLReyesBAS, et al. Elastin insufficiency causes hypertension, structural defects and abnormal remodeling of renal vascular signaling. Kidney Int2017; 92(5): 1100–1118.
58.
TrindadeRAlbrektssonTTengvallP, et al. Foreign body reaction to biomaterials: on mechanisms for buildup and breakdown of osseointegration. Clin Implant Dent Relat Res2016; 18(1): 192–203.
BrownBNBadylakSF.Expanded applications, shifting paradigms and an improved understanding of host–biomaterial interactions. Acta Biomater2013; 9(2): 4948–4955.
