The regeneration of macro-porous electrospun poly(ɛ-caprolactone) vascular graft during long-term in situ implantation
Yifan Wu
Tianjin Key Laboratory of Biomaterial Research, Institute of Biomedical Engineering, Chinese Academy of Medical Sciences and Peking Union Medical College, Tianjin, 300192 China
State Key Laboratory of Medicinal Chemical Biology, Key Laboratory of Bioactive Materials, Ministry of Education, College of Life Science, Nankai University, Tianjin, 300071 China
Search for more papers by this authorYibo Qin
Tianjin Key Laboratory of Biomaterial Research, Institute of Biomedical Engineering, Chinese Academy of Medical Sciences and Peking Union Medical College, Tianjin, 300192 China
Search for more papers by this authorCorresponding Author
Zhihong Wang
Tianjin Key Laboratory of Biomaterial Research, Institute of Biomedical Engineering, Chinese Academy of Medical Sciences and Peking Union Medical College, Tianjin, 300192 China
Correspondence to: D. Kong; e-mail: [email protected] or Z. Wang; e-mail: [email protected]Search for more papers by this authorJianing Wang
State Key Laboratory of Medicinal Chemical Biology, Key Laboratory of Bioactive Materials, Ministry of Education, College of Life Science, Nankai University, Tianjin, 300071 China
Search for more papers by this authorChuangnian Zhang
Tianjin Key Laboratory of Biomaterial Research, Institute of Biomedical Engineering, Chinese Academy of Medical Sciences and Peking Union Medical College, Tianjin, 300192 China
Search for more papers by this authorChen Li
Tianjin Key Laboratory of Biomaterial Research, Institute of Biomedical Engineering, Chinese Academy of Medical Sciences and Peking Union Medical College, Tianjin, 300192 China
Search for more papers by this authorCorresponding Author
Deling Kong
Tianjin Key Laboratory of Biomaterial Research, Institute of Biomedical Engineering, Chinese Academy of Medical Sciences and Peking Union Medical College, Tianjin, 300192 China
State Key Laboratory of Medicinal Chemical Biology, Key Laboratory of Bioactive Materials, Ministry of Education, College of Life Science, Nankai University, Tianjin, 300071 China
Correspondence to: D. Kong; e-mail: [email protected] or Z. Wang; e-mail: [email protected]Search for more papers by this authorYifan Wu
Tianjin Key Laboratory of Biomaterial Research, Institute of Biomedical Engineering, Chinese Academy of Medical Sciences and Peking Union Medical College, Tianjin, 300192 China
State Key Laboratory of Medicinal Chemical Biology, Key Laboratory of Bioactive Materials, Ministry of Education, College of Life Science, Nankai University, Tianjin, 300071 China
Search for more papers by this authorYibo Qin
Tianjin Key Laboratory of Biomaterial Research, Institute of Biomedical Engineering, Chinese Academy of Medical Sciences and Peking Union Medical College, Tianjin, 300192 China
Search for more papers by this authorCorresponding Author
Zhihong Wang
Tianjin Key Laboratory of Biomaterial Research, Institute of Biomedical Engineering, Chinese Academy of Medical Sciences and Peking Union Medical College, Tianjin, 300192 China
Correspondence to: D. Kong; e-mail: [email protected] or Z. Wang; e-mail: [email protected]Search for more papers by this authorJianing Wang
State Key Laboratory of Medicinal Chemical Biology, Key Laboratory of Bioactive Materials, Ministry of Education, College of Life Science, Nankai University, Tianjin, 300071 China
Search for more papers by this authorChuangnian Zhang
Tianjin Key Laboratory of Biomaterial Research, Institute of Biomedical Engineering, Chinese Academy of Medical Sciences and Peking Union Medical College, Tianjin, 300192 China
Search for more papers by this authorChen Li
Tianjin Key Laboratory of Biomaterial Research, Institute of Biomedical Engineering, Chinese Academy of Medical Sciences and Peking Union Medical College, Tianjin, 300192 China
Search for more papers by this authorCorresponding Author
Deling Kong
Tianjin Key Laboratory of Biomaterial Research, Institute of Biomedical Engineering, Chinese Academy of Medical Sciences and Peking Union Medical College, Tianjin, 300192 China
State Key Laboratory of Medicinal Chemical Biology, Key Laboratory of Bioactive Materials, Ministry of Education, College of Life Science, Nankai University, Tianjin, 300071 China
Correspondence to: D. Kong; e-mail: [email protected] or Z. Wang; e-mail: [email protected]Search for more papers by this authorAbstract
Long-term evaluation of vascular grafts is an essential step to facilitate clinical translation. In this study, we investigate the long-term performance of a macro-porous poly(ɛ-caprolactone) (PCL) electrospun vascular graft using the rat abdominal artery replacement model. Long-term patency, endothelialization, and smooth muscle cell regeneration were evaluated, as well as calcification and degradation. The data showed that all the grafts remained open and unobstructed. There was no evidence of aneurysm, stenosis, or calcification one year after implantation. Importantly, neo-vessel was regenerated on the luminal surface of the graft, and was composed of a complete endothelial layer and several layers of smooth muscle cells. The neo-vessel showed vascular physiological function, although not as good as that in native blood vessels, likely due to the remaining scaffold fibers. These data indicated that the PCL macro-porous electrospun vascular graft has potential to be an artery substitute for long-term implantation. Also, this work indicates that continued efforts are needed to develop advanced vascular grafts that exhibit the appropriate balance between the regeneration of the neo-vessel and the complete degradation of the graft materials. © 2017 Wiley Periodicals, Inc. J Biomed Mater Res Part B: Appl Biomater, 106B: 1618–1627, 2018.
REFERENCES
- 1Seifu DG, Purnama A, Mequanint K, Mantovani D. Small-diameter vascular tissue engineering. Nat Rev Cardiol 2013; 10: 410–421.
- 2Song Y, Feijen J, Grijpma DW, Poot AA. Tissue engineering of small-diameter vascular grafts: A literature review. Clin Hemorheol Microcirc 2011; 49: 357–374.
- 3Schmidt CE, Baier JM. Acellular vascular tissues: Natural biomaterials for tissue repair and tissue engineering. Biomaterials 2000; 21: 2215–2231.
- 4Muylaert DE, Fledderus JO, Bouten CV, Dankers PY, Verhaar MC. Combining tissue repair and tissue engineering; bioactivating implantable cell-free vascular scaffolds. Heart 2014; 100: 1825–1830.
- 5Yokoyama U, Tonooka Y, Koretake R, Akimoto T, Gonda Y, Saito J, Umemura M, Fujita T, Sakuma S, Arai F, Kaneko M, Ishikawa Y. Arterial graft with elastic layer structure grown from cells. Sci Rep 2017; 7: 140.
- 6Fukunishi T, Best CA, Ong CS, Groehl T, Reinhardt J, Yi T, Miyachi H, Zhang H, Shinoka T, Breuer CK, Johnson J, Hibino N. Role of bone marrow mononuclear cell seeding for nanofiber vascular grafts. Tissue Eng Part A 2017.
- 7Muylaert DE, van Almen GC, Talacua H, Fledderus JO, Kluin J, Hendrikse SI, van Dongen JL, Sijbesma E, Bosman AW, Mes T, Thakkar SH, Smits AI, Bouten CV, Dankers PY, Verhaar MC. Early in-situ cellularization of a supramolecular vascular graft is modified by synthetic stromal cell-derived factor-1alpha derived peptides. Biomaterials 2016; 76: 187–195.
- 8Caracciolo PC, Rial-Hermida MI, Montini-Ballarin F, Abraham GA, Concheiro A, Alvarez-Lorenzo C. Surface-modified bioresorbable electrospun scaffolds for improving hemocompatibility of vascular grafts. Mater Sci Eng C 2017; 75: 1115–1127.
- 9Savoji H, Maire M, Lequoy P, Liberelle B, De Crescenzo G, Ajji A, Wertheimer MR, Lerouge S. Combining electrospun fiber mats and bioactive coatings for vascular graft prostheses. Biomacromolecules 2017; 18: 303–310.
- 10Qiu X, Lee BL, Ning X, Murthy N, Dong N, Li S. End-point immobilization of heparin on plasma-treated surface of electrospun polycarbonate-urethane vascular graft. Acta Biomater 2017; 51: 138–147.
- 11Brown EE, Hu D, Abu Lail N, Zhang X. Potential of nanocrystalline cellulose-fibrin nanocomposites for artificial vascular graft applications. Biomacromolecules 2013; 14: 1063–1071.
- 12Lu G, Cui SJ, Geng X, Ye L, Chen B, Feng ZG, Zhang J, Li ZZ. Design and preparation of polyurethane-collagen/heparin-conjugated polycaprolactone double-layer bionic small-diameter vascular graft and its preliminary animal tests. China Med J 2013; 126: 1310–1316.
- 13Enayati M, Eilenberg M, Grasl C, Riedl P, Kaun C, Messner B, Walter I, Liska R, Schima H, Wojta J, Podesser BK, Bergmeister H. Biocompatibility assessment of a new biodegradable vascular graft via in vitro co-culture approaches and in vivo model. Ann Biomed Eng 2016; 44: 3319–3334.
10.1007/s10439-016-1601-y Google Scholar
- 14Thottappillil N, Nair PD. Scaffolds in vascular regeneration: Current status. Vasc Health Risk Manage 2015; 11: 79–91.
- 15Xiao Y, Yuan M, Zhang J, Yan J, Lang M. Functional poly(ɛ-caprolactone) based materials: Preparation, self-assembly and application in drug delivery. Curr Top Med Chem 2014; 14: 781–818.
- 16Pohlmann AR, Fonseca FN, Paese K, Detoni CB, Coradini K, Beck RC, Guterres SS. Poly(ɛ-caprolactone) microcapsules and nanocapsules in drug delivery. Expert Opin Drug Delivery 2013; 10: 623–638.
- 17Dash TK, Konkimalla VB. Poly- ɛ-caprolactone based formulations for drug delivery and tissue engineering: A review. J Controlled Release 2012; 158: 15–33.
- 18de Valence S, Tille JC, Mugnai D, Mrowczynski W, Gurny R, Möller M, Walpoth BH. Long term performance of polycaprolactone vascular grafts in a rat abdominal aorta replacement model. Biomaterials 2012; 33: 38–47.
- 19Wang Z, Cui Y, Wang J, Yang X, Wu Y, Wang K, Gao X, Li D, Li Y, Zheng X, Zhu Y, Kong D, Zhao Q. The effect of thick fibers and large pores of electrospun poly(ɛ-caprolactone) vascular grafts on macrophage polarization and arterial regeneration. Biomaterials 2014; 35: 5700–5710.
- 20Wang K, Zhu M, Li T, Zheng W, Li L, Xu M, Zhao Q, Kong D, Wang L. Improvement of cell infiltration in electrospun polycaprolactone scaffolds for the construction of vascular grafts. J Biomed Nanotechnol 2014; 10: 1588–1598.
- 21Zhao Q, Wang S, Kong M, Geng W, Li RK, Song C, Kong D. Phase morphology, physical properties, and biodegradation behavior of novel PLA/PHBHHx blends. J Biomed Mater Res B 2012; 100: 23–31.
- 22Trivedi MK, Sethi KK, Panda P, Jana S. A comprehensive physicochemical, thermal, and spectroscopic characterization of zinc (II) chloride using X-ray diffraction, particle size distribution, differential scanning calorimetry, thermogravimetric analysis/differential thermogravimetric analysis, ultraviolet-visible, and Fourier transform-infrared spectroscopy. Int J Pharm Investig 2017; 7: 33–40.
- 23Gupta P, Kumar M, Bhardwaj N, Kumar JP, Krishnamurthy CS, Nandi SK, Mandal BB. Mimicking form and function of native small diameter vascular conduits using mulberry and non-mulberry patterned silk films. ACS Appl Mater Interfaces 2016; 8: 15874–15888.
- 24Jiang B, Suen R, Wang JJ, Zhang ZJ, Wertheim JA, Ameer GA. Mechanocompatible polymer-extracellular-matrix composites for vascular tissue engineering. Adv Healthcare Mater 2016; 5: 1594–1605.
- 25Zhu M, Wang Z, Zhang J, Wang L, Yang X, Chen J, Fan G, Ji S, Xing C, Wang, Zhao Q, Zhu Y, Kong D, Wang L. Circumferentially aligned fibers guided functional neoartery regeneration in vivo. Biomaterials 2015; 61: 85–94.
- 26Datta P, Ayan B, Ozbolat IT. Bioprinting for vascular and vascularized tissue biofabrication. Acta Biomater 2017; 51: 1–20.
- 27Wang Z, Lu Y, Qin K, Wu Y, Tian Y, Wang J, Zhang J, Hou J, Cui Y, Wang K, Shen J, Xu Q, Kong D, Zhao Q. Enzyme-functionalized vascular grafts catalyze in-situ release of nitric oxide from exogenous NO prodrug. J Controlled Release 2015; 210: 179–188.
- 28Zheng W, Wang Z, Song L, Zhao Q, Zhang J, Li D, Wang S, Han J, Zheng XL, Yang Z, Kong D. Endothelialization and patency of RGD-functionalized vascular grafts in a rabbit carotid artery model. Biomaterials 2012; 33: 2880–2891.
- 29Sarkar S, Schmitz-Rixen T, Hamilton G, Seifalian AM. Achieving the ideal properties for vascular bypass grafts using a tissue engineered approach: A review. Med Biol Eng Comput 2007; 45: 327–336.
- 30Tara S, Kurobe H, Rocco KA, Maxfield MW, Best CA, Yi T, Naito Y, Breuer CK, Shinoka T. Well-organized neointima of large-pore poly(l-lactic acid) vascular graft coated with poly(l-lactic-co-ɛ-caprolactone) prevents calcific deposition compared to small-pore electrospun poly(l-lactic acid) graft in a mouse aortic implantation model. Atherosclerosis 2014; 237: 684–691.
- 31Coombs KE, Leonard AT, Rush MN, Santistevan DA, Hedberg-Dirk EL. Isolated effect of material stiffness on valvular interstitial cell differentiation. J Biomed Mater Res A 2017; 105: 51–61.
- 32Hutcheson JD, Goettsch C, Bertazzo S, Maldonado N, Ruiz JL, Goh W, Yabusaki K, Faits T, Bouten C, Franck G, Quillard T, Libby P, Aikawa M, Weinbaum S, Aikawa E. Genesis and growth of extracellular-vesicle-derived microcalcification in atherosclerotic plaques. Nat Mater 2016; 15: 335–343.
- 33White MP, Rufaihah AJ, Liu L, Ghebremariam YT, Ivey KN, Cooke JP, Srivastava D. Limited gene expression variation in human embryonic stem cell and induced pluripotent stem cell-derived endothelial cells. Stem Cells 2013; 31: 92–103.
- 34Vazão H, Rosa S, Barata T, Costa R, Pitrez PR, Honório I, de Vries MR, Papatsenko D, Benedito R, Saris D, Khademhosseini A, Quax PH, Pereira CF, Mercader N, Fernandes H, Ferreira L. High-throughput identification of small molecules that affect human embryonic vascular development. PNAS 2017; 114: E3022–E3031.