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      Preparation and characterization of small-diameter decellularized scaffolds for vascular tissue engineering in an animal model

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          Abstract

          Background

          The development of a suitable extracellular matrix (ECM) scaffold is the first step in vascular tissue engineering (VTE). Synthetic vascular grafts are available as an alternative to autologous vessels in large-diameter arteries (>8 mm) and medium-diameter arteries (6–8 mm). In small-diameter vessels (<6 mm), synthetic vascular grafts are of limited use due to poor patency rates. Compared with a vascular prosthesis, natural tissue ECM has valuable advantages. Despite considerable progress in recent years, identifying an optimal protocol to create a scaffold for use in small-diameter (<6 mm) fully natural tissue-engineered vascular grafts (TEVG), remains elusive. Although reports on different decellularization techniques have been numerous, combination of and comparison between these methods are scarce; therefore, we have compared five different decellularization protocols for making small-diameter (<6 mm) ECM scaffolds and evaluated their characteristics relative to those of fresh vascular controls.

          Results

          The protocols differed in the choice of enzymatic digestion solvent, the use of non-ionic detergent, the durations of the individual steps, and UV crosslinking. Due to their small diameter and ready availability, rabbit arteria carotis were used as the source of the ECM scaffolds. The scaffolds were subcutaneously implanted in rats and the results were evaluated using various microscopy and immunostaining techniques.

          Conclusions

          Our findings showed that a 2 h digestion time with 1× EDTA, replacing non-ionic detergent with double-distilled water for rinsing and the application of UV crosslinking gave rise to an ECM scaffold with the highest biocompatibility, lowest cytotoxicity and best mechanical properties for use in vivo or in situ pre-clinical research in VTE in comparison.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s12938-017-0344-9) contains supplementary material, which is available to authorized users.

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          Most cited references46

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          An overview of tissue and whole organ decellularization processes.

          Biologic scaffold materials composed of extracellular matrix (ECM) are typically derived by processes that involve decellularization of tissues or organs. Preservation of the complex composition and three-dimensional ultrastructure of the ECM is highly desirable but it is recognized that all methods of decellularization result in disruption of the architecture and potential loss of surface structure and composition. Physical methods and chemical and biologic agents are used in combination to lyse cells, followed by rinsing to remove cell remnants. Effective decellularization methodology is dictated by factors such as tissue density and organization, geometric and biologic properties desired for the end product, and the targeted clinical application. Tissue decellularization with preservation of ECM integrity and bioactivity can be optimized by making educated decisions regarding the agents and techniques utilized during processing. An overview of decellularization methods, their effect upon resulting ECM structure and composition, and recently described perfusion techniques for whole organ decellularization techniques are presented herein. Copyright © 2011 Elsevier Ltd. All rights reserved.
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            Macrophage phenotype and remodeling outcomes in response to biologic scaffolds with and without a cellular component.

            Recently, macrophages have been characterized as having an M1 or M2 phenotype based on receptor expression, cytokine and effector molecule production, and function. The effects of macrophage phenotype upon tissue remodeling following the implantation of a biomaterial are largely unknown. The objectives of this study were to determine the effects of a cellular component within an implanted extracellular matrix (ECM) scaffold upon macrophage phenotype, and to determine the relationship between macrophage phenotype and tissue remodeling. Partial-thickness defects in the abdominal wall musculature of Sprague-Dawley rats were repaired with autologous body wall tissue, acellular allogeneic rat body wall ECM, xenogeneic pig urinary bladder tissue, or acellular xenogeneic pig urinary bladder ECM. At 3, 7, 14, and 28 days the host tissue response was characterized using histologic, immunohistochemical, and RT-PCR methods. The acellular test articles were shown to elicit a predominantly M2 type response and resulted in constructive remodeling, while those containing a cellular component, even an autologous cellular component, elicited a predominantly M1 type response and resulted in deposition of dense connective tissue and/or scarring. We conclude that the presence of cellular material within an ECM scaffold modulates the phenotype of the macrophages participating in the host response following implantation, and that the phenotype of the macrophages participating in the host response appears to be related to tissue remodeling outcome.
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              Functional small-diameter neovessels created using endothelial progenitor cells expanded ex vivo.

              Arterial conduits are increasingly preferred for surgical bypass because of inherent functional properties conferred by arterial endothelial cells, especially nitric oxide production in response to physiologic stimuli. Here we tested whether endothelial progenitor cells (EPCs) can replace arterial endothelial cells and promote patency in tissue-engineered small-diameter blood vessels (4 mm). We isolated EPCs from peripheral blood of sheep, expanded them ex vivo and then seeded them on decellularized porcine iliac vessels. EPC-seeded grafts remained patent for 130 days as a carotid interposition graft in sheep, whereas non-seeded grafts occluded within 15 days. The EPC-explanted grafts exhibited contractile activity and nitric-oxide-mediated vascular relaxation that were similar to native carotid arteries. These results indicate that EPCs can function similarly to arterial endothelial cells and thereby confer longer vascular-graft survival. Due to their unique properties, EPCs might have other general applications for tissue-engineered structures and in treating vascular diseases.
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                Author and article information

                Contributors
                xushuangyue@gmail.com
                lufangna@126.com
                chenglianna@126.com
                allylin521@outlook.com
                xdzhouxu@sina.com
                wuyuan0559@163.com
                596883545@qq.com
                kaichuangzhang@126.com
                luminwang@outlook.com
                xia@xmu.edu.cn
                +86 0592-2187157 , zhuanyiyan@126.com
                +86 0592 2187157 , oti@xmu.edu.cn
                Journal
                Biomed Eng Online
                Biomed Eng Online
                BioMedical Engineering OnLine
                BioMed Central (London )
                1475-925X
                11 May 2017
                11 May 2017
                2017
                : 16
                : 55
                Affiliations
                [1 ]ISNI 0000 0001 2264 7233, GRID grid.12955.3a, , Organ Transplantation Institute of Xiamen University, ; Xiamen, 361102 Fujian Province People’s Republic of China
                [2 ]Fujian Key Laboratory of Organ and Tissue Regeneration, Xiamen, 361102 Fujian Province People’s Republic of China
                [3 ]ISNI 0000 0001 2264 7233, GRID grid.12955.3a, Medical College, , Xiamen University, ; Xiamen, 361000 Fujian Province People’s Republic of China
                [4 ]Cardiovascular Surgery, Heart CenterXiamen University Affiliated Zhongshan Hospital, Xiamen City, 361000 Fujian Province People’s Republic of China
                [5 ]ISNI 0000 0001 2264 7233, GRID grid.12955.3a, Basic Medical Department of Medical College, , Xiamen University, ; Xiamen, 361102 Fujian Province People’s Republic of China
                [6 ]Departmant of Neurosurgery, Fuzhou Second Affiliated Hospital of Xiamen University, Fuzhou, 350007 Fujian Province People’s Republic of China
                [7 ]GRID grid.459700.f, Department of Laboratory Medicine, , Lishui People’s Hospital, ; Lishui, 323000 Zhejiang People’s Republic of China
                Article
                344
                10.1186/s12938-017-0344-9
                5425976
                28494781
                9943c2eb-7853-4cea-a2ae-fbbde15245f4
                © The Author(s) 2017

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 28 December 2016
                : 28 April 2017
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;
                Award ID: 31271038
                Award Recipient :
                Funded by: Major State Scientific Research Program of China
                Award ID: 2012CBA01303
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2017

                Biomedical engineering
                blood vessel decellularization,biocompatibility,arterial tissue engineering,rabbit arteria carotis

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