Research Advances in Regeneration of Soft Tissue with Small Intestinal Submucosa_Journal of Biomedical Engineering

Authors：

Medical School, Ningbo University, Ningbo 315211, China;

Corresponding author：

Keywords：

small intestinal submucosa; extracellular matrix; soft tissue; regenerative medicine; tissue engineering

DOI：

10.7507/1001-5515.20160132

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Small intestinal submucosa (SIS) is a natural decellularized extracellular matrix material. Due to its excellent biocompatibility, unique biomechanical properties and biological activity, it has been widely used as a scaffold in regenerative medicine. This article reviews the recent progress in the characterization and medical application of SIS respectively. The specific biological properties of the SIS, as well as its interaction with cells, are highlighted. Some of the SIS products and clinical cases are also reviewed and discussed.

Citation： ZHUHuangkai, ZHAOJiyuan. Research Advances in Regeneration of Soft Tissue with Small Intestinal Submucosa. Journal of Biomedical Engineering, 2016, 33(4): 816-820. doi: 10.7507/1001-5515.20160132 Copy

1.	LANGER R, VACANTI J P. Tissue engineering[J]. Science, 1993, 260(5110):920-926.
2.	ANDRÁE B, BÄR A, HAVERICH A, et al. Small intestinal submucosa segments as matrix for tissue engineering:review[J]. Tissue Eng Part B Rev, 2013, 19(4):279-291.
3.	CARTER M J, WAYCASTER C, SCHAUM K, et al. Cost-effectiveness of three adjunct cellular/tissue-derived products used in the management of chronic venous leg ulcers[J]. Value Health, 2014, 17(8):801-813.
4.	GLYNN J J, POLSIN E G, HINDS M T. Crosslinking decreases the hemocompatibility of decellularized, porcine small intestinal submucosa[J]. Acta Biomater, 2015, 14(1):96-103.
5.	SHIM S W, KWON D Y, LEE B N, et al. Evaluation of small intestine submucosa and poly(caprolactone-co-lactide) conduits for peripheral nerve regeneration[J]. Tissue Eng Part A, 2015, 21(5-6):1142-1151.
6.	ZAFAR F, HINTON R B, MOORE R A, et al. Physiological growth, remodeling potential, and preserved function of a novel bioprosthetic tricuspid valve:tubular bioprosthesis made of small intestinal submucosa-derived extracellular matrix[J]. J Am Coll Cardiol, 2015, 66(8):877-888.
7.	PADALINO M A, QUARTI A, ANGELI E, et al. Early and mid-term clinical experience with extracellular matrix scaffold for congenital cardiac and vascular reconstructive surgery:a multicentric Italian study[J]. Interact Cardiovasc Thorac Surg, 2015, 21(1):40-49.
8.	ZHANG Fan, LIAO Limin. Tissue engineered cystoplasty augmentation for treatment of neurogenic bladder using small intestinal submucosa:an exploratory study[J]. J Urol, 2014, 192(2):544-550.
9.	NAJI H, FOLEY J, EHREN H. Use of surgisis for abdominal wall reconstruction in children with abdominal wall defects[J]. Eur J Pediatr Surg, 2014, 24(1):94-96.
10.	RAEDER R H, BADYLAK S F, SHEEHAN C, et al. Natural anti-galactose α1, 3 galactose antibodies delay, but do not prevent the acceptance of extracellular matrix xenografts[J]. Transpl Immunol, 2002, 10(1):15-24.
11.	SYED O, WALTERS N J, DAY R M, et al. Evaluation of decellularization protocols for production of tubular small intestine submucosa scaffolds for use in oesophageal tissue engineering[J]. Acta Biomater, 2014, 10(12):5043-5054.
12.	ROEDER R, WOLFE J, LIANAKIS N, et al. Compliance, elastic modulus, and burst pressure of small-intestine submucosa (SIS), small-diameter vascular grafts[J]. J Biomed Mater Res, 1999, 47(1):65-70.
13.	ROPCKE D M, JENSEN M O, JENSEN H, et al. Papillary muscle force distribution after total tricuspid reconstruction using porcine extracellular matrix:in-vitro valve characterization[J]. J Heart Valve Dis, 2014, 23(6):788-794.
14.	SÁNCHEZ-PALENCIA D M, D'AMORE A, GONZÁLEZ-MANCERA A, et al. Effects of fabrication on the mechanics, microstructure and micromechanical environment of small intestinal submucosa scaffolds for vascular tissue engineering[J]. J Biomech, 2014, 47(11):2766-2773.
15.	张承旻.小肠粘膜下层细胞相容性的研究进展[J].大家健康:下旬版, 2013, 7(4):21.
16.	HODONSKY C, MUNDADA L, WANG Shuyun, et al. Effects of scaffold material used in cardiovascular surgery on mesenchymal stem cells and cardiac progenitor cells[J]. Ann Thorac Surg, 2015, 99(2):605-611.
17.	房艳, 倪伟民, 单伟, 等.海绵状的小肠粘膜下层促进成骨样细胞增殖分化[J].中国生物工程杂志, 2013, 33(6):18-23.
18.	BONI L, CHALAJOUR F, SASAKI T, et al. Reconstruction of pulmonary artery with porcine small intestinal submucosa in a lamb surgical model:Viability and growth potential[J]. J Thorac Cardiovasc Surg, 2012, 144(4):963-969.e1; discussion 969.
19.	NAKAO M, UENO T, OGA A, et al. Proposal of intestinal tissue engineering combined with Bianchi's procedure[J]. J Pediatr Surg, 2015, 50(4):573-580.
20.	CHUNG Y G, ALGARRAHI K, FRANCK D, et al. The use of bi-layer silk fibroin scaffolds and small intestinal submucosa matrices to support bladder tissue regeneration in a rat model of spinal cord injury[J]. Biomaterials, 2014, 35(26):7452-7459.
21.	DING Jingxin, ZHANG Xuyin, CHEN Limei, et al. Vaginoplasty using acellular porcine small intestinal submucosa graft in two patients with Meyer-von-Rokitansky-Kuster-Hauser syndrome:a prospective new technique for vaginal reconstruction[J]. Gynecol Obstet Invest, 2013, 75(2):93-96.
22.	FAN Meirong, GONG Mei, DA Lincui, et al. Tissue engineered esophagus scaffold constructed with porcine small intestinal submucosa and synthetic polymers[J]. Biomed Mater, 2014, 9(1):015012.
23.	ZHOU Haiyang, ZHANG Jian, YAN Ronglin, et al. Improving the antibacterial property of porcine small intestinal submucosa by nano-silver supplementation:a promising biological material to address the need for contaminated defect repair[J]. Ann Surg, 2011, 253(5):1033-1041.
24.	ROSSETTO V J, DA MOTA L S, ROCHA N S, et al. Grafts of porcine small intestinal submucosa seeded with cultured homologous smooth muscle cells for bladder repair in dogs[J]. Acta Vet Scand, 2013, 55:39.
25.	POGHOSYAN T, SFEIR R, MICHAUD L, et al. Circumferential esophageal replacement using a tube-shaped tissue-engineered substitute:An experimental study in minipigs[J]. Surgery, 2015, 158(1):266-277.
26.	TAN Bo, WEI Renqian, TAN Meiyun, et al. Tissue engineered esophagus by mesenchymal stem cell seeding for esophageal repair in a canine model[J]. J Surg Res, 2013, 182(1):40-48.
27.	PARK H S, JUNG S Y, KIM H Y, et al. Development of hypoparathyroidism animal model and the feasibility of small intestinal submucosa application on the parathyroid autotransplantation[J]. Eur Arch Otorhinolaryngol, 2015, 272(10):2969-2977.
28.	KIM K, KIM M S. An injectable hydrogel derived from small intestine submucosa as a stem cell carrier[J]. J Biomed Mater Res B Appl Biomater, 2015:doi:10.1002/jbm.b.33504.[Epub ahead of print].
29.	CHOI J W, PARK J K, CHANG J W, et al. Small intestine submucosa and mesenchymal stem cells composite gel for scarless vocal fold regeneration[J]. Biomaterials, 2014, 35(18):4911-4918.
30.	CHOI J S, LEE S, KIM D Y, et al. Functional remodeling after vocal fold injury by small intestinal submucosa gel containing hepatocyte growth factor[J]. Biomaterials, 2015, 40:98-106.
31.	ROW S, PENG Haofan, SCHLAICH E M, et al. Arterial grafts exhibiting unprecedented cellular infiltration and remodeling in vivo: the role of cells in the vascular wall[J]. Biomaterials, 2015, 50:115-126.

1. LANGER R, VACANTI J P. Tissue engineering[J]. Science, 1993, 260(5110):920-926.
2. ANDRÁE B, BÄR A, HAVERICH A, et al. Small intestinal submucosa segments as matrix for tissue engineering:review[J]. Tissue Eng Part B Rev, 2013, 19(4):279-291.
3. CARTER M J, WAYCASTER C, SCHAUM K, et al. Cost-effectiveness of three adjunct cellular/tissue-derived products used in the management of chronic venous leg ulcers[J]. Value Health, 2014, 17(8):801-813.
4. GLYNN J J, POLSIN E G, HINDS M T. Crosslinking decreases the hemocompatibility of decellularized, porcine small intestinal submucosa[J]. Acta Biomater, 2015, 14(1):96-103.
5. SHIM S W, KWON D Y, LEE B N, et al. Evaluation of small intestine submucosa and poly(caprolactone-co-lactide) conduits for peripheral nerve regeneration[J]. Tissue Eng Part A, 2015, 21(5-6):1142-1151.
6. ZAFAR F, HINTON R B, MOORE R A, et al. Physiological growth, remodeling potential, and preserved function of a novel bioprosthetic tricuspid valve:tubular bioprosthesis made of small intestinal submucosa-derived extracellular matrix[J]. J Am Coll Cardiol, 2015, 66(8):877-888.
7. PADALINO M A, QUARTI A, ANGELI E, et al. Early and mid-term clinical experience with extracellular matrix scaffold for congenital cardiac and vascular reconstructive surgery:a multicentric Italian study[J]. Interact Cardiovasc Thorac Surg, 2015, 21(1):40-49.
8. ZHANG Fan, LIAO Limin. Tissue engineered cystoplasty augmentation for treatment of neurogenic bladder using small intestinal submucosa:an exploratory study[J]. J Urol, 2014, 192(2):544-550.
9. NAJI H, FOLEY J, EHREN H. Use of surgisis for abdominal wall reconstruction in children with abdominal wall defects[J]. Eur J Pediatr Surg, 2014, 24(1):94-96.
10. RAEDER R H, BADYLAK S F, SHEEHAN C, et al. Natural anti-galactose α1, 3 galactose antibodies delay, but do not prevent the acceptance of extracellular matrix xenografts[J]. Transpl Immunol, 2002, 10(1):15-24.
11. SYED O, WALTERS N J, DAY R M, et al. Evaluation of decellularization protocols for production of tubular small intestine submucosa scaffolds for use in oesophageal tissue engineering[J]. Acta Biomater, 2014, 10(12):5043-5054.
12. ROEDER R, WOLFE J, LIANAKIS N, et al. Compliance, elastic modulus, and burst pressure of small-intestine submucosa (SIS), small-diameter vascular grafts[J]. J Biomed Mater Res, 1999, 47(1):65-70.
13. ROPCKE D M, JENSEN M O, JENSEN H, et al. Papillary muscle force distribution after total tricuspid reconstruction using porcine extracellular matrix:in-vitro valve characterization[J]. J Heart Valve Dis, 2014, 23(6):788-794.
14. SÁNCHEZ-PALENCIA D M, D'AMORE A, GONZÁLEZ-MANCERA A, et al. Effects of fabrication on the mechanics, microstructure and micromechanical environment of small intestinal submucosa scaffolds for vascular tissue engineering[J]. J Biomech, 2014, 47(11):2766-2773.
15. 张承旻.小肠粘膜下层细胞相容性的研究进展[J].大家健康:下旬版, 2013, 7(4):21.
16. HODONSKY C, MUNDADA L, WANG Shuyun, et al. Effects of scaffold material used in cardiovascular surgery on mesenchymal stem cells and cardiac progenitor cells[J]. Ann Thorac Surg, 2015, 99(2):605-611.
17. 房艳, 倪伟民, 单伟, 等.海绵状的小肠粘膜下层促进成骨样细胞增殖分化[J].中国生物工程杂志, 2013, 33(6):18-23.
18. BONI L, CHALAJOUR F, SASAKI T, et al. Reconstruction of pulmonary artery with porcine small intestinal submucosa in a lamb surgical model:Viability and growth potential[J]. J Thorac Cardiovasc Surg, 2012, 144(4):963-969.e1; discussion 969.
19. NAKAO M, UENO T, OGA A, et al. Proposal of intestinal tissue engineering combined with Bianchi's procedure[J]. J Pediatr Surg, 2015, 50(4):573-580.
20. CHUNG Y G, ALGARRAHI K, FRANCK D, et al. The use of bi-layer silk fibroin scaffolds and small intestinal submucosa matrices to support bladder tissue regeneration in a rat model of spinal cord injury[J]. Biomaterials, 2014, 35(26):7452-7459.
21. DING Jingxin, ZHANG Xuyin, CHEN Limei, et al. Vaginoplasty using acellular porcine small intestinal submucosa graft in two patients with Meyer-von-Rokitansky-Kuster-Hauser syndrome:a prospective new technique for vaginal reconstruction[J]. Gynecol Obstet Invest, 2013, 75(2):93-96.
22. FAN Meirong, GONG Mei, DA Lincui, et al. Tissue engineered esophagus scaffold constructed with porcine small intestinal submucosa and synthetic polymers[J]. Biomed Mater, 2014, 9(1):015012.
23. ZHOU Haiyang, ZHANG Jian, YAN Ronglin, et al. Improving the antibacterial property of porcine small intestinal submucosa by nano-silver supplementation:a promising biological material to address the need for contaminated defect repair[J]. Ann Surg, 2011, 253(5):1033-1041.
24. ROSSETTO V J, DA MOTA L S, ROCHA N S, et al. Grafts of porcine small intestinal submucosa seeded with cultured homologous smooth muscle cells for bladder repair in dogs[J]. Acta Vet Scand, 2013, 55:39.
25. POGHOSYAN T, SFEIR R, MICHAUD L, et al. Circumferential esophageal replacement using a tube-shaped tissue-engineered substitute:An experimental study in minipigs[J]. Surgery, 2015, 158(1):266-277.
26. TAN Bo, WEI Renqian, TAN Meiyun, et al. Tissue engineered esophagus by mesenchymal stem cell seeding for esophageal repair in a canine model[J]. J Surg Res, 2013, 182(1):40-48.
27. PARK H S, JUNG S Y, KIM H Y, et al. Development of hypoparathyroidism animal model and the feasibility of small intestinal submucosa application on the parathyroid autotransplantation[J]. Eur Arch Otorhinolaryngol, 2015, 272(10):2969-2977.
28. KIM K, KIM M S. An injectable hydrogel derived from small intestine submucosa as a stem cell carrier[J]. J Biomed Mater Res B Appl Biomater, 2015:doi:10.1002/jbm.b.33504.[Epub ahead of print].
29. CHOI J W, PARK J K, CHANG J W, et al. Small intestine submucosa and mesenchymal stem cells composite gel for scarless vocal fold regeneration[J]. Biomaterials, 2014, 35(18):4911-4918.
30. CHOI J S, LEE S, KIM D Y, et al. Functional remodeling after vocal fold injury by small intestinal submucosa gel containing hepatocyte growth factor[J]. Biomaterials, 2015, 40:98-106.
31. ROW S, PENG Haofan, SCHLAICH E M, et al. Arterial grafts exhibiting unprecedented cellular infiltration and remodeling in vivo: the role of cells in the vascular wall[J]. Biomaterials, 2015, 50:115-126.

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Research Advances in Regeneration of Soft Tissue with Small Intestinal Submucosa

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