Abstract
To produce an esophageal scaffold with suitable features and evaluate the result of in vivo cell seeding after its implantation in the omentum and near its original anatomical position in the rat model. The esophagus of twelve rats were resected, cannulated, and decellularized via a peristaltic pump. After confirmation of decellularization and preservation of extracellular matrix, decellularized scaffolds were implanted either in the abdominal cavity (group I, n = 6) or cervical area (group II, n = 6). Histological evaluations were performed after 3 and 6 months of implantation. The results of histological evaluations, scanning electron microscopy, and the tensile test confirmed the maintenance of extracellular matrix and removal of all cellular constituents. At the time of biopsy, no evidence of inflammation was detected and the implanted scaffolds appeared normal. Histopathological evaluations of implanted tissues revealed that undifferentiated cells were seen in scaffolds of all follow-ups in both groups. Epithelial cell seeding was more advanced in biopsies of group II obtained after 6 months of operation and was accompanied by angiogenesis in surrounding adventitia. It seems that the implantation of scaffold near its original place may have an important role in further cell seeding. This method may be surpassing in comparison with traditional implantation techniques for perfecting esophageal transplantation.
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Abbreviations
- H&E:
-
Hematoxylin and eosin
- IHC:
-
Immunohistochemistry
- α-SMA:
-
Alpha-smooth muscle actin
- SDS:
-
Sodium dodecyl sulfate
- PBS:
-
Phosphate buffered saline
- ECM:
-
Extra cellular matrix
- SEM:
-
Scanning electron microscopy
References
Chung EJ, Ju HW, Park HJ, Park CH (2015) Three-layered scaffolds for artificial esophagus using poly (ɛ-caprolactone) nanofibers and silk fibroin: an experimental study in a rat model. J Biomed Mater Res Part A 103:2057–2065
Dezawa M et al (2005) Bone marrow stromal cells generate muscle cells and repair muscle degeneration. Science (New York, NY) 309:314–317. https://doi.org/10.1126/science.1110364
Doede T, Bondartschuk M, Joerck C, Schulze E, Goernig M (2009) Unsuccessful alloplastic esophageal replacement with porcine small intestinal submucosa. Artif Organs 33:328–333. https://doi.org/10.1111/j.1525-1594.2009.00727.x
Enzinger PC, Mayer RJ (2003) Esophageal cancer. N Engl J Med 349:2241–2252. https://doi.org/10.1056/NEJMra035010
Freud E, Efrati I, Kidron D, Finally R, Mares AJ (1999) Comparative experimental study of esophageal wall regeneration after prosthetic replacement. J Biomed Mater Res 45:84–91
Green N, Huang Q, Khan L, Battaglia G, Corfe B, MacNeil S, Bury JP (2010) The development and characterization of an organotypic tissue-engineered human esophageal mucosal model. Tissue Eng Part A 16:1053–1064. https://doi.org/10.1089/ten.TEA.2009.0217
Jensen TJ, Foster C, Sayej W, Finck CM (2017) Conditional reprogramming of pediatric human esophageal epithelial cells for use in tissue engineering and disease investigation. J Vis Exp. https://doi.org/10.3791/55243
Johnson CM, Brigger MT (2012) The public health impact of pediatric caustic ingestion injuries. Arch Otolaryngol Head Neck Surg 138:1111–1115. https://doi.org/10.1001/jamaoto.2013.672
Kim IG et al (2019) Tissue-engineered esophagus via bioreactor cultivation for circumferential esophageal reconstruction. Tissue Eng Part A. https://doi.org/10.1089/ten.TEA.2018.0277
Kofler K, Ainoedhofer H, Hollwarth ME, Saxena AK (2010) Fluorescence-activated cell sorting of PCK-26 antigen-positive cells enables selection of ovine esophageal epithelial cells with improved viability on scaffolds for esophagus tissue engineering. Pediatric Surg Int 26:97–104. https://doi.org/10.1007/s00383-009-2512-x
Kuppan P, Sethuraman S, Krishnan UM (2012) Tissue engineering interventions for esophageal disorders—promises and challenges. Biotechnol Adv 30:1481–1492. https://doi.org/10.1016/j.biotechadv.2012.03.005
Laird PW, Zijderveld A, Linders K, Rudnicki MA, Jaenisch R, Berns A (1991) Simplified mammalian DNA isolation procedure. Nucleic Acids Res 19:4293
Liu J, Yang Y, Zheng C, Dong R, Zheng S (2017) Surgical outcomes of different approaches to esophageal replacement in long-gap esophageal atresia: a systematic. Rev Med 96:e6942. https://doi.org/10.1097/md.0000000000006942
Lopes MF, Cabrita A, Ilharco J, Pessa P, Patricio J (2006) Grafts of porcine intestinal submucosa for repair of cervical and abdominal esophageal defects in the rat. J Invest Surg 19:105–111. https://doi.org/10.1080/08941930600569621
Lynen Jansen P, Klinge U, Anurov M, Titkova S, Mertens PR, Jansen M (2004) Surgical mesh as a scaffold for tissue regeneration in the esophagus. Eur Surg Res 36:104–111. https://doi.org/10.1159/000076650
McRorie JW Jr (2018) Heartburn: lifestyle modifications and over-the-counter medications. Nutr Today 53:18–25
Nafisi N et al (2017) Application of human acellular breast dermal matrix (ABDM) in implant-based breast reconstruction: an experimental study. Aesthet Plast Surg 41:1435–1444
Nakase Y et al (2008) Intrathoracic esophageal replacement by in situ tissue-engineered esophagus. J Thorac Cardiovasc Surg 136:850–859. https://doi.org/10.1016/j.jtcvs.2008.05.027
Nguyen DT, Althage M, Magnone MC, Heydarkhan-Hagvall S (2018) Translational strategy: humanized mini-organs. Drug Discov Today. https://doi.org/10.1016/j.drudis.2018.05.039
Orlando G et al (2012) Regeneration and bioengineering of the gastrointestinal tract: current status and future perspectives. Dig Liver Dis 44:714–720. https://doi.org/10.1016/j.dld.2012.04.005
Park SY et al (2016) Tissue-engineered artificial oesophagus patch using three-dimensionally printed polycaprolactone with mesenchymal stem cells: a preliminary report. Interact Cardiovasc Thorac Surg 22:712–717. https://doi.org/10.1093/icvts/ivw048
Poghosyan T, Gaujoux S, Chirica M, Munoz-Bongrand N, Sarfati E, Cattan P (2011) Functional disorders and quality of life after esophagectomy and gastric tube reconstruction for cancer. J Visc Surg 148:e327-335. https://doi.org/10.1016/j.jviscsurg.2011.09.001
Poghosyan T et al (2015) Circumferential esophageal replacement using a tube-shaped tissue-engineered substitute: an experimental study in minipigs. Surgery 158:266–277. https://doi.org/10.1016/j.surg.2015.01.020
Poghosyan T et al (2016) Esophageal tissue engineering: current status and perspectives. J Visc Surg 153:21–29. https://doi.org/10.1016/j.jviscsurg.2015.11.009
Sabetkish S et al (2015) Whole-organ tissue engineering: decellularization and recellularization of three-dimensional matrix liver scaffolds. J Biomed Mater Res Part A 103:1498–1508
Sabetkish S, Sabetkish N, Talebi MA, Halimi S, Kajbafzadeh A-M (2018) The role of nonautologous and autologous adipose-derived mesenchymal stem cell in acute pyelonephritis. Cell Tissue Bank 19:301–309
Saito M, Sakamoto T, Fujimaki M, Tsukada K, Honda T, Nozaki M (2000) Experimental study of an artificial esophagus using a collagen sponge, a latissimus dorsi muscle flap, and split-thickness skin. Surg Today 30:606–613. https://doi.org/10.1007/s005950070100
Saxena AK, Ainoedhofer H, Hollwarth ME (2010) Culture of ovine esophageal epithelial cells and in vitro esophagus tissue engineering. Tissue Eng Part C Methods 16:109–114. https://doi.org/10.1089/ten.TEC.2009.0145
Sharma S, Gupta DK (2017) Surgical techniques for esophageal replacement in children. Pediatr Surg Int 33:527–550. https://doi.org/10.1007/s00383-016-4048-1
Watanabe K, Mark JB (1971) Segmental replacement of the thoracic esophagus with a silastic prosthesis. Am J Surg 121:238–240
Wei RQ et al (2009) Grafts of porcine small intestinal submucosa with cultured autologous oral mucosal epithelial cells for esophageal repair in a canine model. Exp Biol Med (maywood, NJ) 234:453–461. https://doi.org/10.3181/0901-rm-5
Yalcin E, de la Monte S (2016) Tobacco nitrosamines as culprits in disease: mechanisms reviewed. J Physiol Biochem 72:107–120. https://doi.org/10.1007/s13105-016-0465-9
Yamamoto Y et al (1999) Intrathoracic esophageal replacement in the dog with the use of an artificial esophagus composed of a collagen sponge with a double-layered silicone tube. J Thorac Cardiovasc Surg 118:276–286. https://doi.org/10.1016/s0022-5223(99)70218-7
Yamamoto Y et al (2000) Intrathoracic esophageal replacement with a collagen sponge—silicone double layer tube: evaluation of omental-pedicle wrapping and prolonged placement of an inner stent. ASAIO J (Am Soc Artif Internal Org 1992) 46:734–739
Zhu Y, Chian KS, Chan-Park MB, Mhaisalkar PS, Ratner BD (2006) Protein bonding on biodegradable poly(L-lactide-co-caprolactone) membrane for esophageal tissue engineering. Biomaterials 27:68–78. https://doi.org/10.1016/j.biomaterials.2005.05.069
Zhuravleva M et al (2018) In vitro assessment of electrospun polyamide-6 scaffolds for esophageal tissue engineering. J Biomed Mater Res Part B Appl Biomater. https://doi.org/10.1002/jbm.b.34116
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This study was funded by Tehran University of Medical Sciences.
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All animal experiments including animal selection, surgery protocols, and pre-op and post-op care provided for animals were in accordance with the Animal Welfare Act and the Guide for the Care and Use of Laboratory Animals and were approved by the Animal Ethics Committee of the Tehran University of Medical Sciences, School of Medicine and Education, Section of Basic Sciences.
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Eftekharzadeh, S., Akbarzadeh, A., Sabetkish, N. et al. Esophagus tissue engineering: from decellularization to in vivo recellularization in two sites. Cell Tissue Bank 23, 301–312 (2022). https://doi.org/10.1007/s10561-021-09944-6
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DOI: https://doi.org/10.1007/s10561-021-09944-6