Research progress on hydrogels in tissue engineering trachea_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

CHEN Wenxuan ^1,2,3 , SHAN Yibo ^1,2,3 , SUN Fei ^1,2,3 , SHEN Zhiming ^1,2,3 , LU Yi ^1,2,3 , ZHU Jianwei ^1,2,3 , YUAN Lei ^1,2,3 ,  SHI Hongcan ^1,2,3

1. Clinical Medical College, Yangzhou University, Yangzhou, 225009, Jiangsu, P. R. China;
2. Institute of Translational Medicine, Medical College, Yangzhou University, Yangzhou, 225009, Jiangsu, P. R. China;
3. Jiangsu Key Laboratory of Integrated Traditional Chinese and Western Medicine for Prevention and Treatment of Senile Diseases, Yangzhou University, Yangzhou, 225009, Jiangsu, P. R. China;

Corresponding author：

SHI Hongcan, Email: shihongcan@yzu.edu.cn

Keywords：

Hydrogels; trachea; tissue engineering; review

DOI：

10.7507/1007-4848.202305028

Video：

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In cases where a tracheal injury exceeds half the length of the adult trachea or one-third of the length of the child trachea, it becomes difficult to perform end-to-end anastomosis after tracheotomy due to excessive tension at the anastomosis site. In such cases, tracheal replacement therapy is required. Advances in tissue engineering technology have led to the development of tissue engineering tracheal substitutes, which have promising applications. Hydrogels, which are highly hydrated and possess a good three-dimensional network structure, biocompatibility, low immunogenicity, biodegradability, and modifiability, have had wide applications in the field of tissue engineering. This article provides a review of the characteristics, advantages, disadvantages, and effects of various hydrogels commonly used in tissue engineering trachea in recent years. Additionally, the article discusses and offers prospects for the future application of hydrogels in the field of tissue engineering trachea.

1.	Etienne H, Fabre D, Gomez Caro A, et al. Tracheal replacement. Eur Respir J, 2018, 51(2): 1702211.
2.	Ren J, Xu Y, Zhiyi G, et al. Reconstruction of the trachea and carina: Surgical reconstruction, autologous tissue transplantation, allograft transplantation, and bioengineering. Thorac Cancer, 2022, 13(3): 284-295.
3.	Dhasmana A, Singh A, Rawal S. Biomedical grafts for tracheal tissue repairing and regeneration "Tracheal tissue engineering: An overview". J Tissue Eng Regen Med, 2020, 14(5): 653-672.
4.	Slaughter BV, Khurshid SS, Fisher OZ, et al. Hydrogels in regenerative medicine. Adv Mater, 2009, 21(32-33): 3307-3329.
5.	Singh NK, Nguyen QV, Kim BS, et al. Nanostructure controlled sustained delivery of human growth hormone using injectable, biodegradable, pH/temperature responsive nanobiohybrid hydrogel. Nanoscale, 2015, 7(7): 3043-3054.
6.	Sorushanova A, Delgado LM, Wu Z, et al. The collagen suprafamily: From biosynthesis to advanced biomaterial development. Adv Mater, 2019, 31(1): e1801651.
7.	Huang GP, Shanmugasundaram S, Masih P, et al. An investigation of common crosslinking agents on the stability of electrospun collagen scaffolds. J Biomed Mater Res A, 2015, 103(2): 762-771.
8.	Davidenko N, Bax DV, Schuster CF, et al. Optimisation of UV irradiation as a binding site conserving method for crosslinking collagen-based scaffolds. J Mater Sci Mater Med, 2016, 27(1): 14.
9.	Liu HW, Su WT, Liu CY, et al. Highly organized porous gelatin-based scaffold by microfluidic 3D-foaming technology and dynamic culture for cartilage tissue engineering. Int J Mol Sci, 2022, 23(15): 8449.
10.	Xu Y, Wang Z, Hua Y, et al. Photocrosslinked natural hydrogel composed of hyaluronic acid and gelatin enhances cartilage regeneration of decellularized trachea matrix. Mater Sci Eng C Mater Biol Appl, 2021, 120: 111628.
11.	Van Den Bulcke AI, Bogdanov B, De Rooze N, et al. Structural and rheological properties of methacrylamide modified gelatin hydrogels. Biomacromolecules, 2000, 1(1): 31-38.
12.	Tao J, Zhu S, Zhou N, et al. Nanoparticle-stabilized emulsion bioink for digital light processing based 3D bioprinting of porous tissue constructs. Adv Healthc Mater, 2022, 11(12): e2102810.
13.	Zhao Y, Guan J, Wu SJ. Highly stretchable and tough physical silk fibroin-based double network hydrogels. Macromol Rapid Commun, 2019, 40(23): e1900389.
14.	Li T, Song X, Weng C, et al. Enzymatically crosslinked and mechanically tunable silk fibroin/pullulan hydrogels for mesenchymal stem cells delivery. Int J Biol Macromol, 2018, 115: 300-307.
15.	Liu CS, Feng BW, He SR, et al. Preparation and evaluation of a silk fibroin-polycaprolactone biodegradable biomimetic tracheal scaffold. J Biomed Mater Res B Appl Biomater, 2022, 110(6): 1292-1305.
16.	Nematollahi Z, Tafazzoli-Shadpour M, Zamanian A, et al. Fabrication of chitosan silk-based tracheal scaffold using freeze-casting method. Iran Biomed J, 2017, 21(4): 228-239.
17.	Van Bavel N, Lewrenz AM, Issler T, et al. Synthesis of alginate nanoparticles using hydrolyzed and enzyme-digested alginate using the ionic gelation and water-in-oil emulsion method. Polymers (Basel), 2023, 15(5): 1319.
18.	Makarova AO, Derkach SR, Khair T, et al. Ion-induced polysaccharide gelation: Peculiarities of alginate egg-box association with different divalent cations. Polymers (Basel), 2023, 15(5): 1243.
19.	Park JH, Yoon JK, Lee JB, et al. Experimental tracheal replacement using 3-dimensional bioprinted artificial trachea with autologous epithelial cells and chondrocytes. Sci Rep, 2019, 9(1): 2103.
20.	Oprenyeszk F, Sanchez C, Dubuc JE, et al. Chitosan enriched three-dimensional matrix reduces inflammatory and catabolic mediators production by human chondrocytes. PLoS One, 2015, 10(5): e0128362.
21.	Chen H, Wang H, Li B, et al. Enhanced chondrogenic differentiation of human mesenchymal stems cells on citric acid-modified chitosan hydrogel for tracheal cartilage regeneration applications. RSC Adv, 2018, 8(30): 16910-16917.
22.	Kim H, Lee JY, Han H, et al. Improved chondrogenic performance with protective tracheal design of chitosan membrane surrounding 3D-printed trachea. Sci Rep, 2021, 11(1): 9258.
23.	O'Leary C, Soriano L, Fagan-Murphy A, et al. The fabrication and in vitro evaluation of retinoic acid-loaded electrospun composite biomaterials for tracheal tissue regeneration. Front Bioeng Biotechnol, 2020, 8: 190.
24.	Wan T, Fan P, Zhang M, et al. Multiple crosslinking hyaluronic acid hydrogels with improved strength and 3D printability. ACS Appl Bio Mater, 2022, 5(1): 334-343.
25.	Hong HJ, Lee JS, Choi JW, et al. Transplantation of autologous chondrocytes seeded on a fibrin/hyaluronan composite gel into tracheal cartilage defects in rabbits: Preliminary results. Artif Organs, 2012, 36(11): 998-1006.
26.	Hong HJ, Chang JW, Park JK, et al. Tracheal reconstruction using chondrocytes seeded on a poly (L-lactic-co-glycolic acid)-fibrin/hyaluronan. J Biomed Mater Res A, 2014, 102(11): 4142-4150.
27.	Choi JS, Lee MS, Kim J, et al. Hyaluronic acid coating on hydrophobic tracheal scaffold enhances mesenchymal stem cell adhesion and tracheal regeneration. Tissue Eng Regen Med, 2021, 18(2): 225-233.
28.	Uzieliene I, Bironaite D, Pachaleva J, et al. Chondroitin sulfate-tyramine-based hydrogels for cartilage tissue repair. Int J Mol Sci, 2023, 24(4): 3451.
29.	Xu Y, Dai J, Zhu X, et al. Biomimetic trachea engineering via a modular ring strategy based on bone-marrow stem cells and atelocollagen for use in extensive tracheal reconstruction. Adv Mater, 2022, 34(6): e2106755.
30.	Yu X, Qian G, Chen S, et al. A tracheal scaffold of gelatin-chondroitin sulfate-hyaluronan-polyvinyl alcohol with orientated porous structure. Carbohydr Polym, 2017, 159: 20-28.
31.	Huo Y, Xu Y, Wu X, et al. Functional trachea reconstruction using 3D-bioprinted native-like tissue architecture based on designable tissue-specific bioinks. Adv Sci (Weinh), 2022, 9(29): e2202181.
32.	Chang CS, Yang CY, Hsiao HY, et al. Cultivation of auricular chondrocytes in poly (ethylene glycol)/poly (ε-caprolactone) hydrogel for tracheal cartilage tissue engineering in a rabbit model. Eur Cell Mater, 2018, 35: 350-364.
33.	Zhang J, Yang H, Abali BE, et al. Dynamic mechanics-modulated hydrogels to regulate the differentiation of stem-cell spheroids in soft microniches and modeling of the nonlinear behavior. Small, 2019, 15(30): e1901920.

1. Etienne H, Fabre D, Gomez Caro A, et al. Tracheal replacement. Eur Respir J, 2018, 51(2): 1702211.
2. Ren J, Xu Y, Zhiyi G, et al. Reconstruction of the trachea and carina: Surgical reconstruction, autologous tissue transplantation, allograft transplantation, and bioengineering. Thorac Cancer, 2022, 13(3): 284-295.
3. Dhasmana A, Singh A, Rawal S. Biomedical grafts for tracheal tissue repairing and regeneration "Tracheal tissue engineering: An overview". J Tissue Eng Regen Med, 2020, 14(5): 653-672.
4. Slaughter BV, Khurshid SS, Fisher OZ, et al. Hydrogels in regenerative medicine. Adv Mater, 2009, 21(32-33): 3307-3329.
5. Singh NK, Nguyen QV, Kim BS, et al. Nanostructure controlled sustained delivery of human growth hormone using injectable, biodegradable, pH/temperature responsive nanobiohybrid hydrogel. Nanoscale, 2015, 7(7): 3043-3054.
6. Sorushanova A, Delgado LM, Wu Z, et al. The collagen suprafamily: From biosynthesis to advanced biomaterial development. Adv Mater, 2019, 31(1): e1801651.
7. Huang GP, Shanmugasundaram S, Masih P, et al. An investigation of common crosslinking agents on the stability of electrospun collagen scaffolds. J Biomed Mater Res A, 2015, 103(2): 762-771.
8. Davidenko N, Bax DV, Schuster CF, et al. Optimisation of UV irradiation as a binding site conserving method for crosslinking collagen-based scaffolds. J Mater Sci Mater Med, 2016, 27(1): 14.
9. Liu HW, Su WT, Liu CY, et al. Highly organized porous gelatin-based scaffold by microfluidic 3D-foaming technology and dynamic culture for cartilage tissue engineering. Int J Mol Sci, 2022, 23(15): 8449.
10. Xu Y, Wang Z, Hua Y, et al. Photocrosslinked natural hydrogel composed of hyaluronic acid and gelatin enhances cartilage regeneration of decellularized trachea matrix. Mater Sci Eng C Mater Biol Appl, 2021, 120: 111628.
11. Van Den Bulcke AI, Bogdanov B, De Rooze N, et al. Structural and rheological properties of methacrylamide modified gelatin hydrogels. Biomacromolecules, 2000, 1(1): 31-38.
12. Tao J, Zhu S, Zhou N, et al. Nanoparticle-stabilized emulsion bioink for digital light processing based 3D bioprinting of porous tissue constructs. Adv Healthc Mater, 2022, 11(12): e2102810.
13. Zhao Y, Guan J, Wu SJ. Highly stretchable and tough physical silk fibroin-based double network hydrogels. Macromol Rapid Commun, 2019, 40(23): e1900389.
14. Li T, Song X, Weng C, et al. Enzymatically crosslinked and mechanically tunable silk fibroin/pullulan hydrogels for mesenchymal stem cells delivery. Int J Biol Macromol, 2018, 115: 300-307.
15. Liu CS, Feng BW, He SR, et al. Preparation and evaluation of a silk fibroin-polycaprolactone biodegradable biomimetic tracheal scaffold. J Biomed Mater Res B Appl Biomater, 2022, 110(6): 1292-1305.
16. Nematollahi Z, Tafazzoli-Shadpour M, Zamanian A, et al. Fabrication of chitosan silk-based tracheal scaffold using freeze-casting method. Iran Biomed J, 2017, 21(4): 228-239.
17. Van Bavel N, Lewrenz AM, Issler T, et al. Synthesis of alginate nanoparticles using hydrolyzed and enzyme-digested alginate using the ionic gelation and water-in-oil emulsion method. Polymers (Basel), 2023, 15(5): 1319.
18. Makarova AO, Derkach SR, Khair T, et al. Ion-induced polysaccharide gelation: Peculiarities of alginate egg-box association with different divalent cations. Polymers (Basel), 2023, 15(5): 1243.
19. Park JH, Yoon JK, Lee JB, et al. Experimental tracheal replacement using 3-dimensional bioprinted artificial trachea with autologous epithelial cells and chondrocytes. Sci Rep, 2019, 9(1): 2103.
20. Oprenyeszk F, Sanchez C, Dubuc JE, et al. Chitosan enriched three-dimensional matrix reduces inflammatory and catabolic mediators production by human chondrocytes. PLoS One, 2015, 10(5): e0128362.
21. Chen H, Wang H, Li B, et al. Enhanced chondrogenic differentiation of human mesenchymal stems cells on citric acid-modified chitosan hydrogel for tracheal cartilage regeneration applications. RSC Adv, 2018, 8(30): 16910-16917.
22. Kim H, Lee JY, Han H, et al. Improved chondrogenic performance with protective tracheal design of chitosan membrane surrounding 3D-printed trachea. Sci Rep, 2021, 11(1): 9258.
23. O'Leary C, Soriano L, Fagan-Murphy A, et al. The fabrication and in vitro evaluation of retinoic acid-loaded electrospun composite biomaterials for tracheal tissue regeneration. Front Bioeng Biotechnol, 2020, 8: 190.
24. Wan T, Fan P, Zhang M, et al. Multiple crosslinking hyaluronic acid hydrogels with improved strength and 3D printability. ACS Appl Bio Mater, 2022, 5(1): 334-343.
25. Hong HJ, Lee JS, Choi JW, et al. Transplantation of autologous chondrocytes seeded on a fibrin/hyaluronan composite gel into tracheal cartilage defects in rabbits: Preliminary results. Artif Organs, 2012, 36(11): 998-1006.
26. Hong HJ, Chang JW, Park JK, et al. Tracheal reconstruction using chondrocytes seeded on a poly (L-lactic-co-glycolic acid)-fibrin/hyaluronan. J Biomed Mater Res A, 2014, 102(11): 4142-4150.
27. Choi JS, Lee MS, Kim J, et al. Hyaluronic acid coating on hydrophobic tracheal scaffold enhances mesenchymal stem cell adhesion and tracheal regeneration. Tissue Eng Regen Med, 2021, 18(2): 225-233.
28. Uzieliene I, Bironaite D, Pachaleva J, et al. Chondroitin sulfate-tyramine-based hydrogels for cartilage tissue repair. Int J Mol Sci, 2023, 24(4): 3451.
29. Xu Y, Dai J, Zhu X, et al. Biomimetic trachea engineering via a modular ring strategy based on bone-marrow stem cells and atelocollagen for use in extensive tracheal reconstruction. Adv Mater, 2022, 34(6): e2106755.
30. Yu X, Qian G, Chen S, et al. A tracheal scaffold of gelatin-chondroitin sulfate-hyaluronan-polyvinyl alcohol with orientated porous structure. Carbohydr Polym, 2017, 159: 20-28.
31. Huo Y, Xu Y, Wu X, et al. Functional trachea reconstruction using 3D-bioprinted native-like tissue architecture based on designable tissue-specific bioinks. Adv Sci (Weinh), 2022, 9(29): e2202181.
32. Chang CS, Yang CY, Hsiao HY, et al. Cultivation of auricular chondrocytes in poly (ethylene glycol)/poly (ε-caprolactone) hydrogel for tracheal cartilage tissue engineering in a rabbit model. Eur Cell Mater, 2018, 35: 350-364.
33. Zhang J, Yang H, Abali BE, et al. Dynamic mechanics-modulated hydrogels to regulate the differentiation of stem-cell spheroids in soft microniches and modeling of the nonlinear behavior. Small, 2019, 15(30): e1901920.

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