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Cited by 44Tissue Engineering and Regenerative MedicineElectrospun Nanofibers in Biomedical Applications3D Printing in Biomedical Research

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Sonication-Assisted Method for Decellularization of Human Umbilical Artery for Small-Caliber Vascular Tissue Engineering

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Lin, Chih-Hsun, Hsia, Kai, Su, Chih-Kuan, Chen, Chien-Chin, Yeh, Chang-Ching, Ma, Hsu, Lu, Jen-Her·2021·Polymers
DOI 10.3390/polym13111699PMC PMC8196986
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Abstract

Decellularized vascular grafts are useful for the construction of biological small-diameter tissue-engineered vascular grafts (≤6 mm). Traditional chemical decellularization requires a long treatment time, which may damage the structure and alter the mechanical properties. Decellularization using sonication is expected to solve this problem. The aim of this study was to develop an effective decellularization method using ultrasound followed by washing. Different power values of sonication at 40 kHz were tested for 2, 4, and 8 h followed by a washing procedure. The efficacy of sonication of decellularized human umbilical artery (sDHUA) was evaluated via DNA content, histological staining, mechanical properties, and biocompatibility. The sDHUAs were further implanted into rats for up to 90 days and magnetic resonance angiography (MRA) was performed for the implanted grafts. The results demonstrated that treatment of human umbilical artery (HUA) by sonication at ultrasonic power of 204 W for 4 h followed by washing for 24 h in 2% SDS buffer could eliminate more than 90% of cells and retain similar mechanical properties of the HUA. Recellularization was assessed by scanning electron microscopy (SEM), which indicated that sDHUA provided niches for human umbilical vein endothelial cells (HUVECs) to reside, indicating in vitro cytocompatibility. Further implantation tests also indicated the fitness of the sonication-treated HUA as a scaffold for small-caliber tissue engineering vascular grafts.

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Figure 1 Histological stain of HUA, cDHUA, and sDHUA. (A,G,M,S) HUA; (B,H,N,T) cDHUA; (C,I,O,U) sDHUA, 204 W for 4 h; (D,J,P,V) sDHUA, 204 W for 8 h; (E,K,Q,W) sDHUA, 285 W for 2 h; (F,L,R,X) sDHUA, 285 W for 4 h; (A–F) H&E stain; (G–L) DAPI; (M–R) Masson’s trichrome stain; (S–X) Elastin Van Gieson’s stain; Magnification: 200×, Scale bar = 50 μm.
Figure 1 Histological stain of HUA, cDHUA, and sDHUA. (A,G,M,S) HUA; (B,H,N,T) cDHUA; (C,I,O,U) sDHUA, 204 W for 4 h; (D,J,P,V) sDHUA, 204 W for 8 h; (E,K,Q,W) sDHUA, 285 W for 2 h; (F,L,R,X) sDHUA, 285 W for 4 h; (A–F) H&E stain; (G–L) DAPI; (M–R) Masson’s trichrome stain; (S–X) Elastin Van Gieson’s stain; Magnification: 200×, Scale bar = 50 μm.CC BY · PubMed Central
Figure 2 IHC stain of HUA, cDHUA, and sDHUA. (A,G,M,S) HUA; (B,H,N,T) cDHUA; (C,I,O,U) sDHUA, 204 W for 4 h; (D,J,P,V) sDHUA, 204 W for 8 h; (E,K,Q,W) sDHUA, 285 W for 2 h; (F,L,R,X) sDHUA, 285 W for 4 h; (A–F) Collagen type I; (G–L) Collagen type III; (M–R) Fibronectin; (S–X) Laminin; Magnification: 200×, Scale bar = 50 μm.
Figure 2 IHC stain of HUA, cDHUA, and sDHUA. (A,G,M,S) HUA; (B,H,N,T) cDHUA; (C,I,O,U) sDHUA, 204 W for 4 h; (D,J,P,V) sDHUA, 204 W for 8 h; (E,K,Q,W) sDHUA, 285 W for 2 h; (F,L,R,X) sDHUA, 285 W for 4 h; (A–F) Collagen type I; (G–L) Collagen type III; (M–R) Fibronectin; (S–X) Laminin; Magnification: 200×, Scale bar = 50 μm.CC BY · PubMed Central
Figure 3 (a–e): DNA, elastin, GAGs, and collagen content of sDHUA compared with HUA and cDHUA. (A:HUA, B:cDHUA, C:sDHUA, 204 W for 4 h, D:sDHUA, 204 W for 8 h, E:sDHUA, 285 W for 2 h, F:sDHUA, 285 W for 4 h). (a) DNA content (n = 3); (b) elastin content (n = 4); (c) GAG content (n = 4); (d) collagen content (n = 4). (e) Mechanical property (compliance) between HUA, cDHUA, and sDHUA at different pressure. (λ = 1.3). *: p < 0.05, **: p < 0.01, ***: p < 0.005, ****: p < 0.001, ns: no significance.
Figure 3 (a–e): DNA, elastin, GAGs, and collagen content of sDHUA compared with HUA and cDHUA. (A:HUA, B:cDHUA, C:sDHUA, 204 W for 4 h, D:sDHUA, 204 W for 8 h, E:sDHUA, 285 W for 2 h, F:sDHUA, 285 W for 4 h). (a) DNA content (n = 3); (b) elastin content (n = 4); (c) GAG content (n = 4); (d) collagen content (n = 4). (e) Mechanical property (compliance) between HUA, cDHUA, and sDHUA at different pressure. (λ = 1.3). *: p < 0.05, **: p < 0.01, ***: p < 0.005, ****: p < 0.001, ns: no significance.CC BY · PubMed Central
Figure 4 Histological stains of cell seeding sDHUA, 204W for 4 h. (A–D) HUA; (E–H) sDHUA; (I–L) sDHUA seeded with HUVEC; (A,E,I) H&E stain; (B,F,J) DAPI; (C,G,K) CD31; (D,H,L) vWF; Magnification: 200×, Scale bar = 50 μm. L: lumen.
Figure 4 Histological stains of cell seeding sDHUA, 204W for 4 h. (A–D) HUA; (E–H) sDHUA; (I–L) sDHUA seeded with HUVEC; (A,E,I) H&E stain; (B,F,J) DAPI; (C,G,K) CD31; (D,H,L) vWF; Magnification: 200×, Scale bar = 50 μm. L: lumen.CC BY · PubMed Central
Figure 5 SEM of the luminal surface of HUA and sDHUAs seeded with HUVECs. (A,B) HUA, (C–F) sDHUA, 204 W, 4 h, (G–J) sDHUA, 204 W, 8 h, (K–N) sDHUA, 285 W, 2 h, (O–R) sDHUA, 285 W, 4 h. (A,C,G,K,O) Magnification: 2000×, Scale bar = 10 μm; (B,D,H,L,P) Magnification: 10,000×, Scale bar = 1 μm; (E,I,M,Q) Magnification: 800×, Scale bar = 10 μm; (F,J,N,R) Magnification: 2000×, Scale bar = 10 μm.
Figure 5 SEM of the luminal surface of HUA and sDHUAs seeded with HUVECs. (A,B) HUA, (C–F) sDHUA, 204 W, 4 h, (G–J) sDHUA, 204 W, 8 h, (K–N) sDHUA, 285 W, 2 h, (O–R) sDHUA, 285 W, 4 h. (A,C,G,K,O) Magnification: 2000×, Scale bar = 10 μm; (B,D,H,L,P) Magnification: 10,000×, Scale bar = 1 μm; (E,I,M,Q) Magnification: 800×, Scale bar = 10 μm; (F,J,N,R) Magnification: 2000×, Scale bar = 10 μm.CC BY · PubMed Central
Figure 6 sDHUA implantation and MRI image. (A) Gross appearance of the implantation grafts at day-0. (B) Gross appearance of the implantation grafts at day-90. (C) T2 image of coronal view of implantation graft in rat abdominal cavity. (D) T2 image of sagittal view of implantation graft in rat abdominal cavity. (E) TOF 3D display of abdominal artery with the implantation graft. (F) T2 image of coronal view of naïve rat abdominal cavity. (G) T2 image of sagittal view of naïve rat abdominal cavity. (H) TOF 3D display of naïve abdominal artery. (C,D,F,G) Scale bar = 1 cm; Arrow: anastomosis, blue: near the head, yellow: near the tail.
Figure 6 sDHUA implantation and MRI image. (A) Gross appearance of the implantation grafts at day-0. (B) Gross appearance of the implantation grafts at day-90. (C) T2 image of coronal view of implantation graft in rat abdominal cavity. (D) T2 image of sagittal view of implantation graft in rat abdominal cavity. (E) TOF 3D display of abdominal artery with the implantation graft. (F) T2 image of coronal view of naïve rat abdominal cavity. (G) T2 image of sagittal view of naïve rat abdominal cavity. (H) TOF 3D display of naïve abdominal artery. (C,D,F,G) Scale bar = 1 cm; Arrow: anastomosis, blue: near the head, yellow: near the tail.CC BY · PubMed Central
Figure 7 H&E and IHC staining of the explanted grafts at day-30 and day-90. (A–L) day-3; (M–X) day-90; (A,G,M,S) H&E; (B,H,N,T) CD31; (C,I,O,U) vWF; (D,J,P,V) eNOS; (E,K,Q,W) α-SMA; (F,L,R,X) CD45; Red arrow heads in (T,U,V) indicated endothelial cells at inner surface, while red stars marked in W indicated α-SMA-stained cells around sDHUA at day-90. The blue stars indicated sDHUA site. Magnification: (A–F), (M–R) 40×, Scale bar = 200 μm; (G–L,S–X) 200×, Scale bar = 50 μm.
Figure 7 H&E and IHC staining of the explanted grafts at day-30 and day-90. (A–L) day-3; (M–X) day-90; (A,G,M,S) H&E; (B,H,N,T) CD31; (C,I,O,U) vWF; (D,J,P,V) eNOS; (E,K,Q,W) α-SMA; (F,L,R,X) CD45; Red arrow heads in (T,U,V) indicated endothelial cells at inner surface, while red stars marked in W indicated α-SMA-stained cells around sDHUA at day-90. The blue stars indicated sDHUA site. Magnification: (A–F), (M–R) 40×, Scale bar = 200 μm; (G–L,S–X) 200×, Scale bar = 50 μm.CC BY · PubMed Central

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Metadata

Authors
Lin, C.-H., Hsia, K., Su, C.-K., Chen, C.-C., Yeh, C.-C., Ma, H., & Lu, J.-H.
Affiliations
  • National Yang Ming Chiao Tung University (TW)
  • Taipei Veterans General Hospital (TW)
  • Chia-Yi Christian Hospital (TW)
  • Taipei Medical University Hospital (TW)
Corresponding author
Lu, Jen-Her
ORCID
Venue
Polymers
Publisher
MDPI AG
Published
2021-05-22
Volume
13
Issue
11
Pages
1699
ISSN
2073-4360 (ISSN-L)
DOI
10.3390/polym13111699
PMC
PMC8196986
OpenAlex
W3164513037
Cited by
44
References
55
Citations by year
2026: 9 · 2025: 10 · 2024: 13 · 2023: 8 · 2022: 3 · 2021: 1
FWCI
5.87
Type
journal article
Language
en
Open access
Licence
Locations
  • Polymers (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
Ministry of Science and Technology, Taiwan (MoST108-2314-B-075 -053, 108-2314-B-075 -045, and MOST 109-2314-B-075 -007)
Topics
  • Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
  • Physical Sciences › Materials Science › Biomaterials › Electrospun Nanofibers in Biomedical Applications
  • Physical Sciences › Engineering › Biomedical Engineering › 3D Printing in Biomedical Research
Keywords
decellularization, sonication, human umbilical artery, tissue-engineered vascular grafts, small-diameter vascular grafts, ultrasonic power, recellularization, human umbilical vein endothelial cells, graft biocompatibility, graft mechanical properties, graft implantation, magnetic resonance angiography

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Lin, C.-H., Hsia, K., Su, C.-K., Chen, C.-C., Yeh, C.-C., Ma, H., & Lu, J.-H. (2021). Sonication-Assisted Method for Decellularization of Human Umbilical Artery for Small-Caliber Vascular Tissue Engineering. Polymers. https://doi.org/10.3390/polym13111699