Skip to main content

Advertisement

Log in

Intima/medulla reconstruction and vascular contraction–relaxation recovery for acellular small diameter vessels prepared by hyperosmotic electrolyte solution treatment

  • Original Article
  • Tissue Engineering / Regenerative Medicine
  • Published:
Journal of Artificial Organs Aims and scope Submit manuscript

Abstract

This study aims at the evaluation of blood vessel reconstruction process of decellularized small diameter vessels prepared by a hyperosmotic electrolyte solution treatment not only histologically but also physiologically in rat transplantation model. Complete cell removal by a hyperosmotic electrolyte solution treatment was confirmed by hematoxylin/eosin staining and scanning electron microscopic observation. All acellular vessels transplanted into the rat abdominal aorta were patent up to 14 months. One week post-transplantation, the vWF-positive cells were observed on the luminal surface but the layer formation did not complete. Five weeks following transplantation, the vWF-positive endothelial cells were located on the intima consistent with intact endothelial cells. Beneath the endothelial cells, α-SMA-positive smooth muscle cells were distributed. The harvested vessels displayed formation of tunica intima (endothelial cells) and tunica medulla (smooth muscle cell) layers. We also examined the physiological properties of the vessels 12 months post-transplantation using a wire myograph system. The transplanted vessels contracted upon addition of norepinephrine and relaxed upon addition of sodium nitroprusside as well as the native vessels. In conclusion, the acellular vessels prepared with hyperosmotic electrolytic solution showed excellent and long-term patency, which may be related to the successful preservation of vascular ECM. In addition, the acellular vessels revealed the intima/medulla regeneration with the physiological contraction–relaxation functions in response to the each substance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Bosiers M, Torsello G, Gissler HM, Ruef J, Muller-Hulsbeck S, Jahnke T, et al. Nitinol stent implantation in long superficial femoral artery lesions: 12-month results of the DURABILITY I study. J Endovasc Ther. 2009;16:261–9.

    Article  PubMed  Google Scholar 

  2. Chlupac J, Filova E, Bacakova L. Blood vessel replacement: 50 years of development and tissue engineering paradigms in vascular surgery. Physiol Res. 2009;58:S119–39.

    PubMed  Google Scholar 

  3. Schaner PJ, Martin ND, Tulenko TN, Shapiro IM, Tarola NA, Leichter RF, et al. Decellularized vein as a potential scaffold for vascular tissue engineering. J Vasc Surg. 2004;40:146–53.

    Article  PubMed  Google Scholar 

  4. Lin PH, Chen C, Bush RL, Yao Q, Lumsden AB, Hanson SR. Small-caliber heparin-coated ePTFE grafts reduce platelet deposition and neointimal hyperplasia in a baboon model. J Vasc Surg. 2004;39:1322–8.

    Article  PubMed  Google Scholar 

  5. Scott EC, Glickman MH. Conduits for hemodialysis access. Semin Vasc Surg. 2007;20:158–63.

    Article  PubMed  Google Scholar 

  6. Matsumoto H, Hasegawa T, Fuse K, Yamamoto M, Saigusa M. A new vascular prosthesis for a small caliber artery. Surgery. 1973;74:519–23.

    CAS  PubMed  Google Scholar 

  7. Daenens K, Schepers S, Fourneau I, Houthoofd S, Nevelsteen A. Heparin-bonded ePTFE grafts compared with vein grafts in femoropopliteal and femorocrural bypasses: 1- and 2-year results. J Vasc Surg. 2009;49:1210–6.

    Article  PubMed  Google Scholar 

  8. Heyligers JM, Verhagen HJ, Rotmans JI, Weeterings C, de Groot PG, Moll FL, et al. Heparin immobilization reduces thrombogenicity of small-caliber expanded polytetrafluoroethylene grafts. J Vasc Surg. 2006;43:587–91.

    Article  PubMed  Google Scholar 

  9. Hugl B, Nevelsteen A, Daenens K, Perez MA, Heider P, Railo M, et al. PEPE II—a multicenter study with an end-point heparin-bonded expanded polytetrafluoroethylene vascular graft for above and below knee bypass surgery: determinants of patency. J Cardiovasc Surg (Torino). 2009;50:195–203.

    CAS  Google Scholar 

  10. Bader A, Schilling T, Teebken OE, Brandes G, Herden T, Steinhoff G, et al. Tissue engineering of heart valves—human endothelial cell seeding of detergent acellularized porcine valves. Eur J Cardiothorac Surg. 1998;14:279–84.

    Article  CAS  PubMed  Google Scholar 

  11. Yeh HI, Lu SK, Tian TY, Hong RC, Lee WH, Tsai CH. Comparison of endothelial cells grown on different stent materials. J Biomed Mater Res A. 2006;76:835–41.

    Article  PubMed  Google Scholar 

  12. Sreerekha PR, Krishnan LK. Cultivation of endothelial progenitor cells on fibrin matrix and layering on dacron/polytetrafluoroethylene vascular grafts. Artif Organs. 2006;30:242–9.

    Article  CAS  PubMed  Google Scholar 

  13. Cho SW, Jeon O, Lim JE, Gwak SJ, Kim SS, Choi CY, et al. Preliminary experience with tissue engineering of a venous vascular patch by using bone marrow-derived cells and a hybrid biodegradable polymer scaffold. J Vasc Surg. 2006;44:1329–40.

    Article  PubMed  Google Scholar 

  14. Hoerstrup SP, Zund G, Sodian R, Schnell AM, Grunenfelder J, Turina MI. Tissue engineering of small caliber vascular grafts. Eur J Cardiothorac Surg. 2001;20:164–9.

    Article  CAS  PubMed  Google Scholar 

  15. Quint C, Kondo Y, Manson RJ, Lawson JH, Dardik A, Niklason LE. Decellularized tissue-engineered blood vessel as an arterial conduit. Proc Natl Acad Sci USA. 2011;108:9214–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  16. Wu HC, Wang TW, Kang PL, Tsuang YH, Sun JS, Lin FH. Coculture of endothelial and smooth muscle cells on a collagen membrane in the development of a small-diameter vascular graft. Biomaterials. 2007;28:1385–92.

    Article  CAS  PubMed  Google Scholar 

  17. Haruguchi H, Teraoka S. Intimal hyperplasia and hemodynamic factors in arterial bypass and arteriovenous grafts: a review. J Artif Organs. 2003;6:227–35.

    Article  PubMed  Google Scholar 

  18. Lovett M, Eng G, Kluge JA, Cannizzaro C, Vunjak-Novakovic G, Kaplan DL. Tubular silk scaffolds for small diameter vascular grafts. Organogenesis. 2010;6:217–24.

    Article  PubMed Central  PubMed  Google Scholar 

  19. Iwasaki K, Kojima K, Kodama S, Paz AC, Chambers M, Umezu M, et al. Bioengineered three-layered robust and elastic artery using hemodynamically-equivalent pulsatile bioreactor. Circulation. 2008;118:S52–7.

    Article  CAS  PubMed  Google Scholar 

  20. Enomoto S, Sumi M, Kajimoto K, Nakazawa Y, Takahashi R, Takabayashi C, et al. Long-term patency of small-diameter vascular graft made from fibroin, a silk-based biodegradable material. J Vasc Surg. 2010;51:155–64.

    Article  PubMed  Google Scholar 

  21. Nemcova S, Noel AA, Jost CJ, Gloviczki P, Miller VM, Brockbank KG. Evaluation of a xenogeneic acellular collagen matrix as a small-diameter vascular graft in dogs—preliminary observations. J Invest Surg. 2001;14:321–30.

    Article  CAS  PubMed  Google Scholar 

  22. Isenburg JC, Simionescu DT, Vyavahare NR. Elastin stabilization in cardiovascular implants: improved resistance to enzymatic degradation by treatment with tannic acid. Biomaterials. 2004;25:3293–302.

    Article  CAS  PubMed  Google Scholar 

  23. Malone JM, Brendel K, Duhamel RC, Reinert RL. Detergent-extracted small-diameter vascular prostheses. J Vasc Surg. 1984;1:181–91.

    Article  CAS  PubMed  Google Scholar 

  24. Schmidt CE, Baier JM. Acellular vascular tissues: natural biomaterials for tissue repair and tissue engineering. Biomaterials. 2000;21:2215–31.

    Article  CAS  PubMed  Google Scholar 

  25. Teebken OE, Bader A, Steinhoff G, Haverich A. Tissue engineering of vascular grafts: human cell seeding of decellularised porcine matrix. Eur J Vasc Endovasc Surg. 2000;19:381–6.

    Article  CAS  PubMed  Google Scholar 

  26. Wilson GJ, Yeger H, Klement P, Lee JM, Courtman DW. Acellular matrix allograft small caliber vascular prostheses. ASAIO Trans. 1990;36:M340–3.

    CAS  PubMed  Google Scholar 

  27. Yang D, Guo T, Nie C, Morris SF. Tissue-engineered blood vessel graft produced by self-derived cells and allogenic acellular matrix: a functional performance and histologic study. Ann Plast Surg. 2009;62:297–303.

    Article  CAS  PubMed  Google Scholar 

  28. Lalka SG, Oelker LM, Malone JM, Duhamel RC, Kevorkian MA, Raper BA, et al. Acellular vascular matrix: a natural endothelial cell substrate. Ann Vasc Surg. 1989;3:108–17.

    Article  CAS  PubMed  Google Scholar 

  29. Ahn JM, Kim SJ, Kim H, Park C, Kim WH, Park JH. Triton X-100 induces apoptosis in human hepatoma cell lines. Yonsei Med J. 1997;38:52–9.

    CAS  PubMed  Google Scholar 

  30. Ehashi T, Nishigaito A, Fujisato T, Moritan Y, Yamaoka T. Peripheral nerve regeneration and electrophysiological recovery with CIP-treated allogeneic acellular nerves. J Biomater Sci Polym Ed. 2011;22:627–40.

    Article  CAS  PubMed  Google Scholar 

  31. Veith FJ, Moss CM, Sprayregen S, Montefusco C. Preoperative saphenous venography in arterial reconstructive surgery of the lower extremity. Surgery. 1979;85:253–6.

    CAS  PubMed  Google Scholar 

  32. Kawada H, Fujita J, Kinjo K, Matsuzaki Y, Tsuma M, Miyatake H, et al. Nonhematopoietic mesenchymal stem cells can be mobilized and differentiate into cardiomyocytes after myocardial infarction. Blood. 2004;104:3581–7.

    Article  CAS  PubMed  Google Scholar 

  33. Krenning G, Moonen JR, van Luyn MJ, Harmsen MC. Generating new blood flow: integrating developmental biology and tissue engineering. Trends Cardiovasc Med. 2008;18:312–23.

    Article  PubMed  Google Scholar 

  34. Saiura A, Sata M, Hirata Y, Nagai R, Makuuchi M. Circulating smooth muscle progenitor cells contribute to atherosclerosis. Nat Med. 2001;7:382–3.

    Article  CAS  PubMed  Google Scholar 

  35. Haruna Y, Morita Y, Komai N, Yada T, Sakuta T, Tomita N, et al. Endothelial dysfunction in rat adjuvant-induced arthritis: vascular superoxide production by NAD(P)H oxidase and uncoupled endothelial nitric oxide synthase. Arthritis Rheum. 2006;54:1847–55.

    Article  CAS  PubMed  Google Scholar 

  36. Tanaka Y, Mochizuki Y, Tanaka H, Shigenobu K. Significant role of neuronal non-N-type calcium channels in the sympathetic neurogenic contraction of rat mesenteric artery. Br J Pharmacol. 1999;128:1602–8.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  37. Sbitany H, Serletti JM. Acellular dermis-assisted prosthetic breast reconstruction: a systematic and critical review of efficacy and associated morbidity. Plast Reconstr Surg. 2011;128:1162–9.

    Article  CAS  PubMed  Google Scholar 

  38. Glasberg SB, Light D. AlloDerm and Strattice in breast reconstruction: a comparison and techniques for optimizing outcomes. Plast Reconstr Surg. 2012;129:1223–33.

    Article  CAS  PubMed  Google Scholar 

  39. Meyer SR, Chiu B, Churchill TA, Zhu L, Lakey JR, Ross DB. Comparison of aortic valve allograft decellularization techniques in the rat. J Biomed Mater Res A. 2006;79:254–62.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This study was funded by JSPS KAKENHI (Grant Number 22791722). The funding agency received no commercial benefit from this study.

Conflict of interest

The authors have no conflict of interest to declare.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shunsuke Sakakibara.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sakakibara, S., Ishida, Y., Hashikawa, K. et al. Intima/medulla reconstruction and vascular contraction–relaxation recovery for acellular small diameter vessels prepared by hyperosmotic electrolyte solution treatment. J Artif Organs 17, 169–177 (2014). https://doi.org/10.1007/s10047-014-0760-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10047-014-0760-6

Keywords

Navigation