Abstract
Purpose of Review
In the field of tissue engineering, the “perfusion decellularization and recellularization” emerged over the last decade. This technique is generating a complex and perfusable acellular scaffolds (e.g., solid organ) from discarded living tissue. The present work aims to describe all studies in which this technique was applied to complex composite tissues, or one of their elementary tissues.
Recent Findings
A total of 25 experimental publications were found between 2009 and 2020. Studies interested skin/adipose, muscle and nerve flaps for elementary tissues, and larynx, ears, face, upper limbs, uterus, and penis grafts for complex tissue associations. Rat and human models were the most represented.
Summary
This review showed that the current total number of studies covering the entire topic of vascularized composite tissue engineering is only 25, with a majority published within the past 5 years. This promising area of research should be investigated in the future.
Similar content being viewed by others
References
Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance
Rifkin WJ, Bellamy JL, Kantar RS, Farber SJ, Diaz-Siso JR, Brecht LE, et al. Autologous reconstruction of a face transplant candidate. Craniomaxillofac Trauma Reconstr. 2019;12(2):150–5.
Schneeberger S, Petruzzo P, Morelon E, Hautz T, Kanitakis J, Weissenbacher A, et al. 20-year follow-up of two cases of bilateral hand transplantation. N Engl J Med. 2020;383(18):1791–2.
Gilbert Fernandez JJ, Febres-Cordero RG, Simpson RL. The untold story of the first hand transplant: dedicated to the memory of one of the great minds of the ecuadorian medical community and the world. J Reconstr Microsurg. 2019;35(3):163–7.
Dubernard JM, Owen E, Herzberg G, Lanzetta M, Martin X, Kapila H, et al. Human hand allograft: report on first 6 months. Lancet. 1999;353(9161):1315–20.
Brandacher G, Lee WP, Schneeberger S. Minimizing immunosuppression in hand transplantation. Expert Rev Clin Immunol. 2012;8(7):673–83 quiz 84.
Birchall MA, Lorenz RR, Berke GS, Genden EM, Haughey BH, Siemionow M, et al. Laryngeal transplantation in 2005: a review. Am J Transplant. 2006;6(1):20–6.
Dubernard JM, Lengele B, Morelon E, Testelin S, Badet L, Moure C, et al. Outcomes 18 months after the first human partial face transplantation. N Engl J Med. 2007;357(24):2451–60.
Levi DM, Tzakis AG, Kato T, Madariaga J, Mittal NK, Nery J, et al. Transplantation of the abdominal wall. Lancet. 2003;361(9376):2173–6.
Brannstrom M, Johannesson L, Bokstrom H, Kvarnstrom N, Molne J. Dahm-Kahler P, et al. Livebirth after uterus transplantation. 2015;385(9968):607–16.
van der Merwe A, Graewe F, Zuhlke A, Barsdorf NW, Zarrabi AD, Viljoen JT, et al. 2017, Penile allotransplantation for penis amputation following ritual circumcision: a case report with 24 months of follow-up ;390(10099):1038-47.
Szafran AA, Redett R, Burnett AL. Penile transplantation: the US experience and institutional program set-up. Transl Androl Urol. 2018;7(4):639–45.
Dean WK, Talbot SG. Vascularized composite allotransplantation at a crossroad: adopting lessons from technology innovation to novel clinical applications. Transplantation. 2017;101(3):452–6.
Borg T-M, Yalamanchili S, Ghali S, Myers S, Holmes S, Ghanem A. A European perspective of the cost effectiveness of facial composite tissue allotransplantation. Eur J Plast Surg. 2020;43(3):219–24.
Morelon E, Petruzzo P, Kanitakis J, Dakpe S, Thaunat O, Dubois V, et al. Face transplantation: partial graft loss of the first case ten years later. Am J Transplant. 2017;17:1935–40.
Kanitakis J, Petruzzo P, Badet L, Gazarian A, Thaunat O, Testelin S, et al. Chronic rejection in human vascularized composite allotransplantation (hand and face recipients): an update. Transplantation. 2016;100(10):2053–61.
Lantieri L, Cholley B, Lemogne C, Guillemain R, Ortonne N, Grimbert P, et al. 2020, First human facial retransplantation: 30-month follow-up. ;396(10264):1758-65.
Shah Mohammadi M, Buchen JT, Pasquina PF. Niklason L. Jariwala SH. Critical considerations for regeneration of vascularized composite tissues. Tissue Eng Part B Rev: Alvarez LM; 2020.
Pashos NC, Graham DM, Burkett BJ, O’Donnell B, Sabol RA, Helm J, et al. Acellular biologic nipple-areolar complex graft: in vivo murine and nonhuman primate host response evaluation. Tissue Eng Part A. 2020;26:872–85.
Ott HC, Matthiesen TS, Goh SK, Black LD, Kren SM, Netoff TI, et al. Perfusion-decellularized matrix: using nature’s platform to engineer a bioartificial heart. Nat Med. 2008;14(2):213–21.
Peacock EE Jr. Homologous composite tissue grafts of the digital flexor mechanism in human beings. Transplant Bull. 1960;7:418–21.
Ravindra KV, Wu S, Bozulic L, Xu H, Breidenbach WC, Ildstad ST. Composite tissue transplantation: a rapidly advancing field. Transplant Proc. 2008;40(5):1237–48.
Chang EI, Bonillas RG, El-ftesi S, Chang EI, Ceradini DJ, Vial IN, et al. Tissue engineering using autologous microcirculatory beds as vascularized bioscaffolds. FASEB J. 2009;23(3):906–15.
Henderson PW, Nagineni VV, Harper A, Bavinck N, Sohn AM, Krijgh DD, et al. Development of an acellular bioengineered matrix with a dominant vascular pedicle. J Surg Res. 2010;164(1):1–5.
Qu J, Van Hogezand RM, Zhao C, Kuo BJ, Carlsen BT. Decellularization of a fasciocutaneous flap for use as a perfusable scaffold. Ann Plast Surg. 2015;75(1):112–6.
Zhang Q, Johnson JA, Dunne LW, Chen Y, Iyyanki T, Wu Y, et al. Decellularized skin/adipose tissue flap matrix for engineering vascularized composite soft tissue flaps. Acta Biomater. 2016;35:166–84.
Jank BJ, Goverman J, Guyette JP, Charest JM, Randolph M, Gaudette GR, et al. Creation of a bioengineered skin flap scaffold with a perfusable vascular pedicle. Tissue Eng Part A. 2017;23(13-14):696–707.
Giatsidis G, Guyette JP, Ott HC, Orgill DP. Development of a large-volume human-derived adipose acellular allogenic flap by perfusion decellularization. Wound Repair Regen. 2018;26(2):245–50.
Zhang J, Hu ZQ, Turner NJ, Teng SF, Cheng WY, Zhou HY, et al. Perfusion-decellularized skeletal muscle as a three-dimensional scaffold with a vascular network template. Biomaterials. 2016;89:114–26.
Sabbagh MD, Roh SG, Liu J, Morsy M, Abu-Ghname A, Zhao C, et al. A quick and reliable method to decellularize a gracilis flap: a crucial step toward building a muscle. Ann Plast Surg. 2019;83(6):709–15.
Wuthrich T, Lese I, Haberthur D, Zubler C, Hlushchuk R, Hewer E, et al. Development of vascularized nerve scaffold using perfusion-decellularization and recellularization. Mater Sci Eng C Mater Biol Appl. 2020;117:111311.
Hou N, Cui P, Luo J, Ma R, Zhu L. Tissue-engineered larynx using perfusion-decellularized technique and mesenchymal stem cells in a rabbit model. Acta Otolaryngol. 2011;131(6):645–52.
Ma R, Li M, Luo J, Yu H, Sun Y, Cheng S, et al. Structural integrity, ECM components and immunogenicity of decellularized laryngeal scaffold with preserved cartilage. Biomaterials. 2013;34(7):1790–8.
Moser PT, Gerli M, Diercks GR, Evangelista-Leite D, Charest JM, Gershlak JR, et al. Creation of laryngeal grafts from primary human cells and decellularized laryngeal scaffolds. Tissue Eng Part A. 2020;26(9-10):543–55.
Duisit J, Orlando G, Debluts D, Maistriaux L, Xhema D, de Bisthoven YJ, et al. Decellularization of the porcine ear generates a biocompatible, nonimmunogenic extracellular matrix platform for face subunit bioengineering. Ann Surg. 2017.
Duisit J, Amiel H, Wuthrich T, Taddeo A, Dedriche A, Destoop V, et al. Perfusion-decellularization of human ear grafts enables ECM-based scaffolds for auricular vascularized composite tissue engineering. Acta Biomater. 2018;73:339–54.
Duisit J, Amiel H, Orlando G, Dedriche A, Behets C, Gianello P, et al. Face graft scaffold production in a rat model. Plast Reconstr Surg. 2018;141(1):95–103.
Duisit J, Maistriaux L, Taddeo A, Orlando G, Joris V, Coche E, et al. Bioengineering a human face graft: the matrix of identity. Ann Surg. 2017;266:754–64.
Jank BJ, Xiong L, Moser PT, Guyette JP, Ren X, Cetrulo CL, et al. Engineered composite tissue as a bioartificial limb graft. Biomaterials. 2015;61:246–56.
Gerli MFM, Guyette JP, Evangelista-Leite D, Ghoshhajra BB, Ott HC. Perfusion decellularization of a human limb: a novel platform for composite tissue engineering and reconstructive surgery. PLoS One. 2018;13(1):e0191497.
Tan Y, Landford WN, Garza M, Suarez A, Zhou Z, Coon D. Complete human penile scaffold for composite tissue engineering: organ decellularization and characterization. Sci Rep. 2019;9(1):16368.
Hellstrom M, El-Akouri RR, Sihlbom C, Olsson BM, Lengqvist J, Backdahl H, et al. Towards the development of a bioengineered uterus: comparison of different protocols for rat uterus decellularization. Acta Biomater. 2014;10(12):5034–42.
Miyazaki K, Maruyama T. Partial regeneration and reconstruction of the rat uterus through recellularization of a decellularized uterine matrix. Biomaterials. 2014;35(31):8791–800.
Campo H, Baptista PM, Lopez-Perez N, Faus A, Cervello I, Simon C. De- and recellularization of the pig uterus: a bioengineering pilot study. Biol Reprod. 2017;96(1):34–45.
Padma AM, Tiemann TT, Alshaikh AB, Akouri R, Song MJ, Hellstrom M, Protocols for rat uterus isolation and decellularization: applications for uterus tissue engineering and 3D cell culturing 2018;1577:161-175.
Daryabari SS, Kajbafzadeh AM, Fendereski K, Ghorbani F, Dehnavi M, Rostami M, et al. Development of an efficient perfusion-based protocol for whole-organ decellularization of the ovine uterus as a human-sized model and in vivo application of the bioscaffolds. J Assist Reprod Genet. 2019;36(6):1211–23.
Tiemann TT, Padma AM, Sehic E, Backdahl H, Oltean M, Song MJ, et al. Towards uterus tissue engineering: a comparative study of sheep uterus decellularisation. Mol Hum Reprod. 2020;26(3):167–78.
Kajbafzadeh AM, Khorramirouz R, Akbarzadeh A, Sabetkish S, Sabetkish N, Saadat P, et al. A novel technique for simultaneous whole-body and multi-organ decellularization: umbilical artery catheterization as a perfusion-based method in a sheep foetus model. Int J Exp Pathol. 2015;96(2):116–32.
Cao Y, Vacanti JP, Paige KT, Upton J, Vacanti CA. Transplantation of chondrocytes utilizing a polymer-cell construct to produce tissue-engineered cartilage in the shape of a human ear. Plast Reconstr Surg. 1997;100(2):297–302 discussion 3-4.
Clites TR, Carty MJ, Ullauri JB, Carney ME, Mooney LM, Duval J-F, et al. Proprioception from a neurally controlled lower-extremity prosthesis. Sci Transl Med. 2018;10(443):eaap8373.
Duisit J, Maistriaux L, Gerdom A, Vergauwen M, Gianello P, Behets C, et al. Nose and lip graft variants: a subunit anatomical study. Plast Reconstr Surg. 2018;141(3):751–61.
Davidson EH, Wang EW, Yu JY, Fernandez-Miranda JC, Wang DJ, Richards N, et al. Total human eye allotransplantation: developing surgical protocols for donor and recipient procedures. Plast Reconstr Surg. 2016;138(6):1297–308.
Badylak S. Perspective: work with, not against, biology. Nature. 2016;540(7632):S55.
Acknowledgements
JD is supported by Fonds de Recherche Clinique (FRC), Cliniques Universitaires Saint-Luc/UCLouvain grant. LM is a “Fonds National de La Recherche Scientifique” (FNRS, Belgium) research fellow
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
All reported studies/experiments with human or animal subjects performed by the authors have been previously published and complied with all applicable ethical standards (including the Helsinki declaration and its amendments, institutional/national research committee standards, and international/national/institutional guidelines).
Conflict of Interest
The authors declare no competing interests.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
This article is part of the Topical Collection on Cellular Transplant
Rights and permissions
About this article
Cite this article
Duisit, J., Maistriaux, L., Bertheuil, N. et al. Engineering Vascularized Composite Tissues by Perfusion Decellularization/Recellularization: Review. Curr Transpl Rep 8, 44–56 (2021). https://doi.org/10.1007/s40472-021-00317-2
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40472-021-00317-2