The effect of decellularization of tracheal allografts on leukocyte infiltration and of recellularization on regulatory T cell recruitment
Abstract
Tracheal transplantation without immunosuppressive therapy has been accomplished with a tissue-engineering approach using decellularized biological scaffolds in combination with recipient progenitor cells. The mechanisms of immune response directed towards these tracheal allografts have not been fully determined. In this study, we evaluated the immunogenicity of these grafts at the protein level, and functionally, in vitro and in vivo in a large animal model. Long-segment circumferential tracheal allografts were decellularized using two different protocols and recellularized using recipient mesenchymal stromal cells (MSC) and tracheal epithelial progenitor cells (TEC). Residual MHCI and MHCII immunostaining was found surrounding the submucosal glands despite cyclical decellularization. In an in vitro lymphocyte proliferation assay, CD4+ T cells continued to proliferate on decellularized pieces and this proliferation was inhibited by co-culture with autologous MSC. Allografts were heterotopically transplanted under a muscle flap in the neck of the recipients and decellularization was found to delay leukocyte infiltration but resulted in eventual cartilage degradation. Recellularization prevented this infiltration up to 3 weeks post-transplantation and allowed for preservation of the cartilage. The immune cells found within these grafts included a significant number of CD4+CD25+Foxp3+ regulatory T cells. Furthermore, gene expression of anti-inflammatory cytokines, such as IL-10 and TGF-β1, involved in proliferation, differentiation and function of regulatory T cells was found in these grafts. These results indicate that the immunological modification induced by recellularized tracheal scaffolds is an active process involving the recruitment of immunosuppressive cells, rather than simply the removal of donor-derived antigenic components.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
dECM-based scaffolds are more biocompatible and confront less rejection rate compared to other implants.
“Thereby, dECM-based scaffolds are more biocompatible and confront less rejection rate compared to other implants [30–32].”
From Immunogenicity of decellularized extracellular matrix scaffolds: a bottleneck in tissue engineering and regenerative medicine (2023) · cites this paper as [30]
dECM scaffolds affect CD4+ T cell maturation and differentiation to shift T cell polarization toward regulatory phenotype (T reg), an immunomodulatory subtype that downregulates T cell activity.
“dECM scaffolds affect CD4+ T cell maturation and differentiation to shift T cell polarization toward regulatory phenotype (T reg), an immunomodulatory subtype that downregulates T cell activity.”
From Immunogenicity of decellularized extracellular matrix scaffolds: a bottleneck in tissue engineering and regenerative medicine (2023) · cites this paper as [30]
Cites
2 retracted
RETRACTED: Clinical transplantation of a tissue-engineered airway
Macchiarini, P., Jungebluth, P., Go, T., Asnaghi, M. A., Rees, L., Cogan, T. A., Dodson, A., Martorell, J., Bellini, S., Parnigotto, P. P., et al. (2008) · The Lancet · doi:10.1016/s0140-6736(08)61598-6 · Cited by 1,431 · see citing works
RetractedMesenchymal stromal cells for tissue-engineered tissue and organ replacements
Baiguera, S., Jungebluth, P., Mazzanti, B., & Macchiarini, P. (2012) · Transplant International · doi:10.1111/j.1432-2277.2011.01426.x · Cited by 40 · see citing works
RetractedMesenchymal stem cells in health and disease
Uccelli, A., Moretta, L., & Pistoia, V. (2008) · Nature reviews. Immunology · doi:10.1038/nri2395 · Cited by 3,750 · see citing works
Decellularization of tissues and organs
Gilbert, T. W., Sellaro, T. L., & Badylak, S. F. (2006) · Biomaterials · doi:10.1016/j.biomaterials.2006.02.014 · Cited by 2,222 · see citing works
TRANSFORMING GROWTH FACTOR-β REGULATION OF IMMUNE RESPONSES
Li, M. O., Wan, Y. Y., Sanjabi, S., Robertson, A.-K. L., & Flavell, R. A. (2005) · Annual Review of Immunology · doi:10.1146/annurev.immunol.24.021605.090737 · Cited by 2,199 · see citing works
Kehrl, J. H., Wakefield, L. M., Roberts, A. B., Jakowlew, S. B., Álvarez‐Mon, M., Derynck, R., Sporn, M. B., & Fauci, A. S. (1986) · The Journal of Experimental Medicine · doi:10.1084/jem.163.5.1037 · Cited by 1,581 · see citing works
Immune response to biologic scaffold materials
Badylak, S. F., & Gilbert, T. W. (2008) · Seminars in Immunology · doi:10.1016/j.smim.2007.11.003 · Cited by 857 · see citing works
Macrophage Phenotype as a Determinant of Biologic Scaffold Remodeling
Badylak, S. F., Valentin, J. E., Ravindra, A. K., McCabe, G. P., & Stewart-Akers, A. M. (2008) · Tissue Engineering Part A · doi:10.1089/ten.tea.2007.0264 · Cited by 729 · see citing works
Potential role of interleukin-10-secreting regulatory T cells in allergy and asthma
Hawrylowicz, C. M., & O’Garra, A. (2005) · Nature reviews. Immunology · doi:10.1038/nri1589 · Cited by 682 · see citing works
Consequences of ineffective decellularization of biologic scaffolds on the host response
Keane, T. J., Londono, R., Turner, N. J., & Badylak, S. F. (2012) · Biomaterials · doi:10.1016/j.biomaterials.2011.10.054 · Cited by 613 · see citing works
Thompson, N. L., Flanders, K. C., Smith, J. M., Ellingsworth, L. R., Roberts, A. B., & Sporn, M. B. (1989) · The Journal of Cell Biology · doi:10.1083/jcb.108.2.661 · Cited by 448 · see citing works
Strategies for use of IL‐10 or its antagonists in human disease
O’Garra, A., Barrat, F. J., Castro, A. G., Vicari, A. P., & Hawrylowicz, C. M. (2008) · Immunological Reviews · doi:10.1111/j.1600-065x.2008.00635.x · Cited by 445 · see citing works
Casiraghi, F., Azzollini, N., Cassis, P., Imberti, B., Morigi, M., Cugini, D., Cavinato, R. A., Todeschini, M., Solini, S., Sonzogni, A., et al. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.181.6.3933 · Cited by 423 · see citing works
Ge, W., Jiang, J., Arp, J., Liu, W., Garcia, B. M., & Wang, H. (2010) · Transplantation · doi:10.1097/tp.0b013e3181fed001 · Cited by 350 · see citing works
Substrate Rigidity Regulates Human T Cell Activation and Proliferation
O’Connor, R. S., Hao, X., Shen, K., Bashour, K. T., Akimova, T., Hancock, W. W., Kam, L. C., & Milone, M. C. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1102757 · Cited by 331 · see citing works
Ge, W., Jiang, J., Baroja, M. L., Arp, J., Zassoko, R., Liu, W., Bartholomew, A. M., García, B., & Wang, H. (2009) · American Journal of Transplantation · doi:10.1111/j.1600-6143.2009.02721.x · Cited by 271 · see citing works
[Surgery of the trachea and bronchi].
Hc, G. (1987) · PubMed · Cited by 201 · see citing works
Conconi, M. T., Coppi, P. D., Liddo, R. D., Vigolo, S., Zanon, G. F., Parnigotto, P. P., & Nussdorfer, G. G. (2005) · Transplant International · doi:10.1111/j.1432-2277.2005.00082.x · Cited by 175 · see citing works
Bosch, P., Pratt, S. L., & Stice, S. L. (2005) · Biology of Reproduction · doi:10.1095/biolreprod.105.045138 · Cited by 164 · see citing works
Smyth, M. J., Strobl, S., Young, H. A., Ortaldo, J. R., & Ochoa, A. C. (1991) · The Journal of Immunology · doi:10.4049/jimmunol.146.10.3289 · Cited by 160 · see citing works
Go, T., Jungebluth, P., Baiguero, S., Asnaghi, M. A., Martorell, J., Ostertag, H., Mantero, S., Birchall, M., Bader, A., & Macchiarini, P. (2009) · Journal of Thoracic and Cardiovascular Surgery · doi:10.1016/j.jtcvs.2009.10.002 · Cited by 155 · see citing works
22 week assessment of bladder acellular matrix as a bladder augmentation material in a porcine model
Brown, A., Farhat, W. A., Merguerian, P. A., Wilson, G. J., Khoury, A. E., & Woodhouse, K. A. (2002) · Biomaterials · doi:10.1016/s0142-9612(01)00350-7 · Cited by 152 · see citing works
Hydrated xenogeneic decellularized tracheal matrix as a scaffold for tracheal reconstruction
Remlinger, N. T., Czajka, C. A., Juhas, M. E., Vorp, D. A., Stolz, D. B., Badylak, S. F., Gilbert, S., & Gilbert, T. W. (2010) · Biomaterials · doi:10.1016/j.biomaterials.2010.01.067 · Cited by 140 · see citing works
Wilshaw, S.-P., Kearney, J., Fisher, J., & Ingham, E. (2008) · Tissue Engineering Part A · doi:10.1089/tea.2007.0145 · Cited by 137 · see citing works
Jungebluth, P., Go, T., Asnaghi, M. A., Bellini, S., Martorell, J., Calore, C., Urbani, L., Ostertag, H., Mantero, S., Conconi, M. T., et al. (2009) · Journal of Thoracic and Cardiovascular Surgery · doi:10.1016/j.jtcvs.2008.09.085 · Cited by 128 · see citing works
Surgery of the Trachea and Bronchi
Pearson, F. G. (2005) · The Annals of Thoracic Surgery · doi:10.1016/j.athoracsur.2004.08.052 · Cited by 120 · see citing works
Recellularization of Decellularized Allograft Scaffolds in Ovine Great Vessel Reconstructions
Ketchedjian, A., Jones, A. L., Krueger, P. M., Robinson, E., Crouch, K., Wolfinbarger, L., & Hopkins, R. A. (2005) · The Annals of Thoracic Surgery · doi:10.1016/j.athoracsur.2004.09.033 · Cited by 118 · see citing works
Decellularization reduces the immune response to aortic valve allografts in the rat
Meyer, S. R., Nagendran, J., Desai, L. S., Rayat, G. R., Churchill, T. A., Anderson, C. C., Rajotte, R. V., Lakey, J. R. T., & Ross, D. B. (2005) · Journal of Thoracic and Cardiovascular Surgery · doi:10.1016/j.jtcvs.2005.03.021 · Cited by 117 · see citing works
McKarns, S. C., & Schwartz, R. H. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.4.2071 · Cited by 112 · see citing works
Novel Utilization of Serum in Tissue Decellularization
Gui, L., Chan, S. A., Breuer, C. K., & Niklason, L. E. (2010) · Tissue Engineering Part C: Methods · doi:10.1089/ten.tec.2009.0120 · Cited by 109 · see citing works
Böer, U., Lohrenz, A., Klingenberg, M., Pich, A., Haverich, A., & Wilhelmi, M. (2011) · Biomaterials · doi:10.1016/j.biomaterials.2011.09.015 · Cited by 107 · see citing works
TGFβ1 and Treg cells: alliance for tolerance
Bommireddy, R., & Doetschman, T. (2007) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2007.08.005 · Cited by 102 · see citing works
Moving towards in situ tracheal regeneration: the bionic tissue engineered transplantation approach
Bader, A., & Macchiarini, P. (2010) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2010.01073.x · Cited by 96 · see citing works
Bayrak, A., Tyralla, M., Ladhoff, J., Schleicher, M., Stock, U. A., Volk, H.-D., & Seifert, M. (2010) · Biomaterials · doi:10.1016/j.biomaterials.2010.01.120 · Cited by 96 · see citing works
Merguerian, P. A., Reddy, P. P., Barrieras, D., Wilson, G. J., Woodhouse, K. A., Bägli, D., McLorie, G. A., & Khoury, A. E. (2000) · British Journal of Urology · doi:10.1046/j.1464-410x.2000.00513.x · Cited by 90 · see citing works
Haykal, S., Soleas, J. P., Salna, M. P., Hofer, S. O. P., & Waddell, T. K. (2012) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2011.0579 · Cited by 86 · see citing works
Self-citationTGF-β1 Regulates Differentiation of Bone Marrow Mesenchymal Stem Cells
Zhao, L., & Hantash, B. M. (2011) · Vitamins and hormones · doi:10.1016/b978-0-12-386015-6.00042-1 · Cited by 86 · see citing works
Engela, A. U., Baan, C. C., Dor, F. J. M. F., Weimar, W., & Hoogduijn, M. J. (2012) · Frontiers in Immunology · doi:10.3389/fimmu.2012.00126 · Cited by 82 · see citing works
Ma, R., Li, M., Luo, J., Yu, H., Sun, Y., Cheng, S.-Y., & Cui, P. (2012) · Biomaterials · doi:10.1016/j.biomaterials.2012.11.026 · Cited by 81 · see citing works
Morphologic Assessment of Extracellular Matrix Scaffolds for Patch Tracheoplasty in a Canine Model
Gilbert, T. W., Gilbert, S., Madden, M., Reynolds, S. D., & Badylak, S. F. (2008) · The Annals of Thoracic Surgery · doi:10.1016/j.athoracsur.2008.04.071 · Cited by 80 · see citing works
The concept of in vivo airway tissue engineering
Jungebluth, P., Bader, A., Baiguera, S., Möller, S., Jaus, M. O., Lim, M. L., Fried, K., Kjartansdóttir, K. R., Go, T., Nave, H., et al. (2012) · Biomaterials · doi:10.1016/j.biomaterials.2012.03.016 · Cited by 74 · see citing works
Raghavan, S. S., Woon, C. Y. L., Kraus, A., Megerle, K., Choi, M. S. S., Pridgen, B. C., Pham, H., & Chang, J. (2012) · Tissue Engineering Part A · doi:10.1089/ten.tea.2011.0422 · Cited by 71 · see citing works
Bastian, F., Stelzmüller, M.-E., Kratochwill, K., Kasimir, M.-T., Simon, P., & Weigel, G. (2008) · Biomaterials · doi:10.1016/j.biomaterials.2008.01.005 · Cited by 47 · see citing works
Mechanisms of tolerance and allergic sensitization in the airways and the lungs
de Lafaille, M. A. C., Lafaille, J. J., & Graça, L. (2010) · Current Opinion in Immunology · doi:10.1016/j.coi.2010.08.014 · Cited by 39 · see citing works
Guo-feng, L. I. U., He, Z., Yang, D., Han, X., Guo, T., Hao, C., Ma, H., & Nie, C. (2008) · Chinese Medical Journal · doi:10.1097/00029330-200808010-00013 · Cited by 38 · see citing works
Transforming growth factor‐β in allergic inflammatory disease of the upper airways: friend or foe?
Salib, R. J., & Howarth, P. H. (2009) · Clinical & Experimental Allergy · doi:10.1111/j.1365-2222.2009.03239.x · Cited by 26 · see citing works
Liu, Y., Nakamura, T., Yamamoto, Y., Matsumoto, K., Sekine, T., Ueda, H. R., & Shimizu, Y. (2000) · ASAIO Journal · doi:10.1097/00002480-200009000-00005 · Cited by 24 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Vascular Tissue Engineering: Progress, Challenges, and Clinical Promise
Song, H.-H. G., Rumma, R. T., Ozaki, C. K., Edelman, E. R., & Chen, C. S. (2018) · Cell Stem Cell · doi:10.1016/j.stem.2018.02.009 · Cited by 476 · see citing works
Kasravi, M., Ahmadi, A., Babajani, A., Mazloomnejad, R., Hatamnejad, M. R., Shariatzadeh, S., Bahrami, S., & Niknejad, H. (2023) · Biomaterials Research · doi:10.1186/s40824-023-00348-z · Cited by 316 · see citing works
Extracellular Matrix-Based Biomaterials and Their Influence Upon Cell Behavior
Cramer, M. C., & Badylak, S. F. (2020) · Annals of Biomedical Engineering · doi:10.1007/s10439-019-02408-9 · Cited by 196 · see citing works
The host response to naturally-derived extracellular matrix biomaterials
Morris, A. H., Stamer, D. K., & Kyriakides, T. R. (2017) · Seminars in Immunology · doi:10.1016/j.smim.2017.01.002 · Cited by 180 · see citing works
Beheshtizadeh, N., Gharibshahian, M., Pazhouhnia, Z., Rostami, M., Zangi, A. R., Maleki, R., Azar, H. K., Zalouli, V., Rajavand, H., Farzin, A., et al. (2022) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2022.113431 · Cited by 98 · see citing works
Rowland, C. R., Glass, K. A., Ettyreddy, A. R., Gloss, C. C., Matthews, J. R. L., Huynh, N. P. T., & Guilak, F. (2018) · Biomaterials · doi:10.1016/j.biomaterials.2018.04.049 · Cited by 92 · see citing works
Chandra, P. K., & Atala, A. (2019) · Clinical Science · doi:10.1042/cs20180155 · Cited by 91 · see citing works
Airway tissue engineering: an update
Fishman, J. M., Wiles, K., Lowdell, M. W., Coppi, P. D., Elliott, M. J., Atala, A., & Birchall, M. (2014) · Expert Opinion on Biological Therapy · doi:10.1517/14712598.2014.938631 · Cited by 85 · see citing works
Decellularized Tooth Bud Scaffolds for Tooth Regeneration
Zhang, W., Vazquez, B., Oreadi, D., & Yelick, P. C. (2017) · Journal of Dental Research · doi:10.1177/0022034516689082 · Cited by 84 · see citing works
Xu, M., Su, T., Jin, X., Li, Y., Yao, Y., Liu, K., Chen, K., Lu, F., & He, Y. (2022) · Acta Biomaterialia · doi:10.1016/j.actbio.2022.08.015 · Cited by 84 · see citing works
The Host Immune Response to Tissue-Engineered Organs: Current Problems and Future Directions
Wiles, K., Fishman, J. M., Coppi, P. D., & Birchall, M. (2015) · Tissue Engineering Part B Reviews · doi:10.1089/ten.teb.2015.0376 · Cited by 81 · see citing works
Lama, V. N., Belperio, J. A., Christie, J. D., El‐Chemaly, S., Fishbein, M. C., Gelman, A. E., Hancock, W. W., Keshavjee, S. H., Kreisel, D., Laubach, V. E., et al. (2017) · JCI Insight · doi:10.1172/jci.insight.93121 · Cited by 81 · see citing works
Extracellular matrix scaffold-immune microenvironment modulates tissue regeneration
Yu, Y., Zhang, W., Liu, X., Wang, H., Shen, J., Xiao, H., Mei, J., Chai, Y., & Wen, G. (2021) · Composites Part B Engineering · doi:10.1016/j.compositesb.2021.109524 · Cited by 63 · see citing works
Park, J., Park, J. Y., Nam, I., Hwang, S. H., Kim, C., Jung, J. W., Jang, J., Lee, H., Choi, Y., Park, S. H., et al. (2015) · Acta Biomaterialia · doi:10.1016/j.actbio.2015.07.014 · Cited by 61 · see citing works
Automation of Pressure Control Improves Whole Porcine Heart Decellularization
Momtahan, N., Poornejad, N., Struk, J. A., Castleton, A. A., Herrod, B. J., Vance, B. R., Eatough, J. P., Roeder, B. L., Reynolds, P. R., & Cook, A. D. (2015) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2014.0709 · Cited by 59 · see citing works
Decellularized cartilage as a prospective scaffold for cartilage repair
Xia, C., Mei, S., Gu, C., Zheng, L., Chen, F., Shi, Y., Wu, K., Lu, T., Jin, Y., Lin, X., et al. (2019) · Materials Science and Engineering C · doi:10.1016/j.msec.2019.04.002 · Cited by 57 · see citing works
Regulator Versus Effector Paradigm: Interleukin-10 as Indicator of the Switching Response
Mingomataj, E., & Bakiri, A. H. (2015) · Clinical Reviews in Allergy & Immunology · doi:10.1007/s12016-015-8514-7 · Cited by 54 · see citing works
De-epithelialization of porcine tracheal allografts as an approach for tracheal tissue engineering
Aoki, F. G., Varma, R., Marin‐Araujo, A. E., Lee, H., Soleas, J. P., Li, A. H., Soon, K., Romero, D. A., Moriya, H. T., Haykal, S., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-48450-4 · Cited by 54 · see citing works
Self-citationHaykal, S., Salna, M. P., Zhou, Y., Marcus, P., Fatehi, M., Frost, G., Machuca, T., Hofer, S. O. P., & Waddell, T. K. (2014) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2013.0627 · Cited by 49 · see citing works
Self-citationSobreiro‐Almeida, R., Quinteira, R., & Neves, N. M. (2021) · Advanced Healthcare Materials · doi:10.1002/adhm.202100160 · Cited by 49 · see citing works
Multipotent Stromal Cells Outperform Chondrocytes on Cartilage-Derived Matrix Scaffolds
Benders, K. E. M., Boot, W., Cokelaere, S. M., van Weeren, P. R., Gawlitta, D., Bergman, H. J., Saris, D. B. F., Dhert, W. J. A., & Malda, J. (2014) · Cartilage · doi:10.1177/1947603514535245 · Cited by 47 · see citing works
The Challenge in Using Mesenchymal Stromal Cells for Recellularization of Decellularized Cartilage
Huang, Z., Godkin, O., & Schulze-Tanzil, G. G. (2016) · Stem Cell Reviews and Reports · doi:10.1007/s12015-016-9699-8 · Cited by 43 · see citing works
Autologous Cell Seeding in Tracheal Tissue Engineering
Maughan, E. F., Hynds, R. E., Proctor, T. J., Janes, S. M., Elliott, M. J., Birchall, M., Lowdell, M. W., & Coppi, P. D. (2017) · Current Stem Cell Reports · doi:10.1007/s40778-017-0108-2 · Cited by 42 · see citing works
Momtahan, N., Sukavaneshvar, S., Roeder, B. L., & Cook, A. D. (2014) · Tissue Engineering Part B Reviews · doi:10.1089/ten.teb.2014.0192 · Cited by 41 · see citing works
Recellularization of Native Tissue Derived Acellular Scaffolds with Mesenchymal Stem Cells
Ahmed, E., Saleh, T., & Xu, M. (2021) · Cells · doi:10.3390/cells10071787 · Cited by 40 · see citing works
Weiss, D. J., Elliott, M. J., Jang, Q., Poole, B. R., & Birchall, M. (2014) · Cytotherapy · doi:10.1016/j.jcyt.2014.10.012 · Cited by 37 · see citing works
Herrmann, P., Ansari, T., Southgate, A., Varanou, A., Partington, L., Carvalho, C., Janes, S. M., Lowdell, M. W., Sibbons, P. D., & Birchall, M. (2017) · Journal of Tissue Engineering and Regenerative Medicine · doi:10.1002/term.2596 · Cited by 36 · see citing works
Tracheal Tissue Engineering: Principles and State of the Art
Mammana, M., Bonis, A., Verzeletti, V., Dell’Amore, A., & Rea, F. (2024) · Bioengineering · doi:10.3390/bioengineering11020198 · Cited by 31 · see citing works
Ostadi, Y., Khanali, J., Tehrani, F. A., Yazdanpanah, G., Bahrami, S., Niazi, F., & Niknejad, H. (2024) · Biomaterials Research · doi:10.34133/bmr.0071 · Cited by 30 · see citing works
Fishman, J. M., Wiles, K., & Wood, K. J. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-800196-7.00008-6 · Cited by 28 · see citing works
Hondt, M. D., Vanaudenaerde, B. M., Maughan, E. F., Butler, C. R., Crowley, C., Verbeken, E. K., Verleden, S. E., & Vranckx, J. J. (2017) · Acta Biomaterialia · doi:10.1016/j.actbio.2017.07.035 · Cited by 27 · see citing works
Lee, H., Marin‐Araujo, A. E., Aoki, F. G., Haykal, S., Waddell, T. K., Amon, C. H., Romero, D. A., & Karoubi, G. (2021) · Scientific Reports · doi:10.1038/s41598-020-80841-w · Cited by 24 · see citing works
Self-citationProgress and Current Limitations of Materials for Artificial Bile Duct Engineering
Sun, Q., Shen, Z., Liang, X., He, Y., Kong, D., Midgley, A. C., & Wang, K. (2021) · Materials · doi:10.3390/ma14237468 · Cited by 21 · see citing works
Decellularized tracheal scaffolds in tracheal reconstruction: An evaluation of different techniques
Lei, C., Mei, S., Zhou, C. H., & Xia, C. (2021) · Journal of Applied Biomaterials & Functional Materials · doi:10.1177/22808000211064948 · Cited by 20 · see citing works
Reconstruction of Anterior Tracheal Defects Using a Bioengineered Graft in a Porcine Model
Al‐Ayoubi, A. M., Rehmani, S. S., Sinclair, C. F., Lebovics, R. S., & Bhora, F. Y. (2016) · The Annals of Thoracic Surgery · doi:10.1016/j.athoracsur.2016.10.034 · Cited by 20 · see citing works
Xu, Y. F., Li, Y., Liu, Y., Li, H., Jia, Z., Tang, Y., Jiang, G., Zhang, X., & Duan, L. (2019) · PubMed Central · Cited by 19 · see citing works
Decellularization techniques: unveiling the blueprint for tracheal tissue engineering
Gomes, K. T., Prasad, P. R., Sandhu, J. S., Kumar, A., Kumar, N. A. N., Shridhar, N., Bisht, B., & Paul, M. K. (2025) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2025.1518905 · Cited by 15 · see citing works
Tissue Engineering for Tracheal Replacement: Strategies and Challenges
Samat, A. A., Hamid, Z. A. A., Mustapha, M. J. @., & Yahaya, B. H. (2022) · Advances in experimental medicine and biology · doi:10.1007/5584_2022_707 · Cited by 14 · see citing works
Pai, A. C., Lynch, T. J., Ahlers, B. A., Ievlev, V., Engelhardt, J. F., & Parekh, K. R. (2022) · Cells · doi:10.3390/cells11061027 · Cited by 14 · see citing works
Epithelial grafting of a decellularized whole-tracheal segment: an in vivo experimental model
Hondt, M. D., Vanaudenaerde, B. M., Verbeken, E. K., & Vranckx, J. J. (2017) · Interactive Cardiovascular and Thoracic Surgery · doi:10.1093/icvts/ivx442 · Cited by 13 · see citing works
Trachea Engineering Using a Centrifugation Method and Mouse-Induced Pluripotent Stem Cells
Zhou, Q., Ye, X., Ran, Q., Kitahara, A., Matsumoto, Y., Moriyama, M., Ajioka, Y., & Saijo, Y. (2018) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2018.0115 · Cited by 12 · see citing works
Szulc, D. A., Ahmadipour, M., Aoki, F. G., Waddell, T. K., Karoubi, G., & Cheng, H. M. (2019) · Magnetic Resonance in Medicine · doi:10.1002/mrm.28072 · Cited by 12 · see citing works
Self-citationA fibrin‐coated pericardial extracellular matrix prevented heart adhesion in a rat model
Funamoto, S., Hashimoto, Y., Kishida, A., & Negishi, J. (2018) · Journal of Biomedical Materials Research Part B Applied Biomaterials · doi:10.1002/jbm.b.34201 · Cited by 10 · see citing works
de Wit, R., Siddiqi, S., Tiemessen, D. M., Snabel, R. R., Veenstra, G. J. C., Oosterwijk, E., & Verhagen, A. F. T. M. (2021) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.16916 · Cited by 10 · see citing works
Future directions for research on tissue-engineered trachea
Tang, H., Sun, W., Chen, Y., She, Y., & Chen, C. (2022) · Bio-Design and Manufacturing · doi:10.1007/s42242-022-00193-4 · Cited by 6 · see citing works
Arakélian, L., Léger, M., Kellouche, S., Agniel, R., Bruneval, P., Allain, J., Caputo, V., Gendron, N., Gozlan, R., Bargui, R., et al. (2024) · Advanced Biology · doi:10.1002/adbi.202400208 · Cited by 4 · see citing works
Decellularized Scaffolds for Tissue Regeneration: Techniques and Applications
Biazar, E. (2024) · Biomedical engineering · doi:10.5772/intechopen.1007748 · Cited by 4 · see citing works
Prophylactic use of antimicrobials in surgical pig models; a literature review (2012‐2014)
Bradbury, A. G., Argyle, S. A., Eddleston, M., & Clutton, R. E. (2015) · Veterinary Record · doi:10.1136/vr.103043 · Cited by 3 · see citing works
Tracheal Regeneration: Recent Progress in the Application of Stem Cells in Tracheal Bioengineering
Ganji, F., Billan, F. L., Haykal, S., & Karoubi, G. (2026) · International Journal of Molecular Sciences · doi:10.3390/ijms27062891 · Cited by 2 · see citing works
Self-citationEvaluation of a decellularized bronchial patch transplant in a porcine model
Taniguchi, D., Kamata, S., Rostami, S., Tuin, S. A., Marin‐Araujo, A. E., Guthrie, K., Petersen, T. H., Waddell, T. K., Karoubi, G., Keshavjee, S. H., et al. (2023) · Scientific Reports · doi:10.1038/s41598-023-48643-y · Cited by 2 · see citing works
Self-citationLeón-Félix, C. M., Sousa, R. L., Bols, P. E. J., & Appeltant, R. (2026) · Cell and Tissue Research · doi:10.1007/s00441-026-04068-3 · Cited by 1 · see citing works
Zhou, K. X., Aoki, F. G., Marin, A., Karoubi, G., Haykal, S., & Waddell, T. K. (2023) · International Journal of Medical Students · doi:10.5195/ijms.2023.1437 · Cited by 1 · see citing works
Self-citationLee, H. (2019) · TSpace (University of Toronto) · Cited by 1 · see citing works
Mardani, R. (2020) · TSpace (University of Toronto) · Cited by 1 · see citing works
Hanaki, S., Takao, T., Fujisawa, Y., Ota, T., Osone, T., Otake, S., Iwai, R., Deguchi, K., Yamamoto, K., Okuyama, H., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.06.05.654989
Tracheal graft engineering: State of the art
Duru, Ç., & Haykal, S. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-30084-4.00013-2
Self-citation
- Authors
- Haykal, S., Zhou, Y., Marcus, P., Salna, M., Machuca, T., Hofer, S. O. P., & Waddell, T. K.
- Affiliations
- University Health Network (CA)
- University of Toronto (CA)
- Corresponding author
- Waddell, Thomas K.
- Venue
- Biomaterials
- Publisher
- Elsevier BV
- Published
- 2013-07
- Volume
- 34
- Issue
- 23
- Pages
- 5821-5832
- ISSN
- 0142-9612 (ISSN-L)
- OpenAlex
- W2083881520
- Cited by
- 59
- References
- 47
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 4 · 2023: 3 · 2022: 5 · 2021: 9 · 2020: 1 · 2019: 7 · 2018: 4 · 2017: 7 · 2016: 2 · 2015: 6 · 2014: 6
- FWCI
- 4.59
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- Locations
- Biomaterials (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
- Health Sciences › Medicine › Transplantation › Organ and Tissue Transplantation Research
- Health Sciences › Medicine › Surgery › Transplantation: Methods and Outcomes
- Keywords
- tracheal transplantation, decellularization, recellularization, tracheal allograft, leukocyte infiltration, regulatory T cells, mesenchymal stem cells, immunogenicity, MHC expression, CD4+ T cell proliferation, cartilage degeneration, anti-inflammatory cytokines, IL-10, TGF-β1, immunosuppression
- MeSH terms
- Animals, Histocompatibility Antigens Class II, Epithelial Cells, Immunohistochemistry, Lymphocyte Activation, Male, Phenotype, Trachea, Transplantation, Homologous, Histocompatibility Antigens Class I, Transplantation, Heterotopic, Cytokines, Coculture Techniques, Sus scrofa, Cell Proliferation, T-Lymphocytes, Regulatory, Mesenchymal Stem Cells, Allografts
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
