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Experimental Assessment of Small Intestinal Submucosa As a Small Bowel Graft in a Rat Model

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Experimental Assessment of Small Intestinal Submucosa As a Small Bowel Graft in a Rat Model Experimental Assessment of Small Intestinal Submucosa as a Small Bowel Graft in a Rat Model By Zhong Qiu Wang, Yasuhiro Watanabe, and Akira Toki Kagawa, Japan Background/Purpose: Small intestinal submucosa (SIS) is an tion was evident, but the luminal surface was not epithelized. extracellular matrix used in tissue engineering. The purpose By 4 weeks, transitional mucosal epithelial layer began to of this study is to evaluate the feasibility of using SIS as a line the luminal surface of the graft, and nearly 70% luminal scafford for small bowel regeneration in a rat model. surface of the graft had been covered by mucosal epithelium at 8 weeks. By 12 weeks, the luminal surface was covered Methods: A 2-cm length tubular SIS graft from donor completely by a mucosal layer with distinct bundles of Sprague Dawley rats was interposed with bilateral anasto- smooth muscle cells in the neointestine. At 24 weeks, the mosis in the median tract of an isolated ileal loop of Lewis neointestine wall showed 3 layers of mucosa, smooth mus- rats used to construct an ileostomy. The grafts were har- cle, and serosa. vested and analyzed at each of the time-points ranging from 2 weeks to 24 weeks after operation using histology and Conclusions: The preliminary study suggested that SIS allow immunohistochemistry. rapid regeneration of mucosa and smooth muscle and might Results: Macroscopic examination found no adhesion in the be a viable material for the creation of neointestine. surrounding area of neointestine by 24 weeks, and no ste- J Pediatr Surg 38:1596-1601. © 2003 Elsevier Inc. All rights nosis was visible. The shrinkage of neointestine was indi- reserved. cated from 20% to 40%. Histologic and immunohistochemi- cal evaluation showed that SIS grafts were colonized by INDEX WORDS: Small bowel, tissue engineering, small in- numerous inflammation cells by 2 weeks. Neovasculariza- testinal submucosa. HORT BOWEL syndrome is defined as the spectrum man is still limited by unsolved immunologic problems7,8 S of malabsorption that occurs after resection of a and organ donor shortage especially among the pediatric major portion of the small intestine.1-3 It is suggested that population.9 many patients with short bowel syndrome are dependent Small intestinal submucosa (SIS) is a membrane har- on total parenteral nutrition (TPN) and cannot be weaned vesting from the animal small intestine after which the off TPN because of the extensive resection or inadequate tunica mucosa, serosa, and muscularis are removed, adaptation.4 This type of nutrition support is associated providing a collagen-rich membrane that is composed with recurrent episodes of systemic infection and pro- mainly of the submucosal layer.10,11 SIS is unique from gressive cholestatic live disease. In addition, home-based other previously used graft materials in that it contains TPN is accompanied by expensive costs estimated at functional growth factors that are likely vital to the 12 approximately $100,000 per year.5 Surgical treatment of regenerative process. SIS has been shown to be bio- short bowel syndrome at bowel lengthening or slowing compatible, resistant to infection, and induce tissue- specific regeneration in numerous tissues, including the intestinal transit to increase the absorptive surface area or blood vessels, the abdominal wall, urinary bladder, and time has been unsuccessful.4,6,7 Small bowel transplan- tendons.10,13-15 SIS also has undergone serial immuno- tation as a promising treatment option has been promoted logic testing, and there has not been any evidence of for patients with life-threatening complications from rejection reaction.16-18 TPN. However, use of small bowel transplantation in The investigation in tissue engineering for bioengi- neering small bowel has been initiated using biomaterials 19,20 From the Department of Pediatric Surgery, Kagawa Medical Uni- like SIS or polyglycolic acid by Vacanti and others. The versity Faculty of Medicine, Kagawa, Japan. current study addresses the suitability of SIS grafts used as Supported by grants from the Scientific Research Fund of Minister of a scaffold for small bowel regeneration in the rat model. Education, Science and Culture of Japan (grant C11671771). Address reprint requests to Zhong Qiu Wang, MD, PhD, Department of Pediatric Surgery, Kagawa Medical University Faculty of Medicine, MATERIALS AND METHODS 1750-1, Miki, Kita-gun, Kagawa, 761-07 Japan. Animal Care © 2003 Elsevier Inc. All rights reserved. 0022-3468/03/3811-0007$30.00/0 All animal care and use complied with the institutional regulations doi:10.1016/S0022-3468(03)00567-0 established and approved by the Animal Care and Use Committee of 1596 Journal of Pediatric Surgery, Vol 38, No 11 (November), 2003: pp 1596-1601 SIS BOWEL GRAFTS 1597 Kagawa Medical University for Animal Research Program. Sprague Dawley and Lewis rats were used in this study. Rats were kept in individual cages and fed standard rat chow and water ad libitum for a period of 1 week before use. Surgical procedures were performed under fluothane inhalational anesthesia. Preparation of Small Intestinal Submucosa Male Sprague Dawley rats were used as donors for the source of SIS. SIS was prepared as outlined previously in detail by Badylak et al.13 In brief, segments of rat intestine were harvested and immediately placed in 0.9% saline solution. Segments then were cut into 2-cm lengths, and the mesenteric tissues were removed carefully from the segments. The segment of intestine then was everted (inside out), and the superficial mucosa was removed mechanically using a scalpel handle and moist- ened gauze. The segment then was everted again with the stratum compactum becoming the new luminal lining, as in its original orien- tation, and the serosal and muscularis layers were removed from its outer surface by the similar mechanical abrasion. This produces an Fig 2. A double ileostomy at either side of the abdominal midline extremely thin, translucent, whitish membrane tube (diameter, 4 to 6 at 8 weeks. Some luminal contents were excreted from the stoma mm) consisting of the submucosa with the attached stratum compactum (arrowhead). and muscularis mucosa of the mucosa. The SIS then was rinsed with saline. To construct a multilayered tube, 4 layers of SIS were wrapped on a 6-mm diameter plastic tube and sewed at the edges of the SIS 12 weeks and then removed. Loop washes were performed with saline together with absorbable sutures. The SIS grafts then were sterilized in solution through the ileostomy one time every other day for more than 75% ethanol, rinsed in saline solution again, and stored at 4°Cina10% 12 weeks. neomycin sulfate (Sigma, St Louis, MO) solution until use. Storage time for the SIS grafts ranged from 1 week to 3 months. Specimen Assessment Scheduled euthanization was carried out at various time points SIS Implantation ranging from 2 to 24 weeks. The specimens were harvested, and the Adult male Lewis rats (n ϭ 20) were used as recipients for this silk suture area along with luminal size was measured. The specimens project. Under fluothane inhalational anesthesia, a midline abdominal then were submitted for histologic, histochemical, and immunohisto- incision was made, and the abdominal cavity was exposed. An ileal chemical assessment. Specimens were fixed in formalin, dehydrated, loop with several vascular vessels was isolated, whereas the interrupted and embedded in paraffin wax. Sections were cut at 4 ␮ m and stained bowel was reanastomosed to maintain the normal alimentary canal. A with H&E and Masson’s trichrome stains. The presence of smooth 2-cm in length tubular SIS graft was interposed in the median tract of muscle cells and innervation of remodeling graft were checked by the ileal loop and anastomosed in an end-to-end fashion using inter- immunohischemical staining using monoclonal mouse antihuman rupted 7-0 absorbable polydioxanone sutures (Fig 1). Two to 4 silk ␣-smooth muscle actin antibody (Dako Corp, Carpinteria, CA) and sutures were added to the anastomosis to act as a marker for later antiS100 (Sigma, St Louis, MO). Sections were dewaxed and rehy- identification. Before completion of anastomosis, a silicon stent was drated. After the endogenous peroxidase activity blocking, sections placed in the loop. The ileal loop then was used to construct a double were incubated with a primary antibody diluted 1:1000 for 10 minutes ileostomy at each side of the abdominal incision (Fig 2). The abdominal with the LSAB2 systems (Dako Corp, Carpinteria, CA). Sections then incision was closed in 2 layers with 4-0 nylons. were washed, and the antibody binding sites were revealed by incu- Postoperatively, animals were maintained on a liquid diet and water bating the sections in a solution of diaminobenzidine hydrochloride for 48 hours and then recommenced on a full diet of rat chow. (DAB) (Dako Corp, Carpinteria, CA). The normal intestinal smooth Antibiotics were used for 1 week. The loop stent was kept in place for muscle was stained as a positive control. RESULTS Of the 20 animals receiving the SIS grafts implanta- tions, 2 rats were killed within 2 weeks owing to the operative complications related to stenosis or peritonitis secondary to the leakage at the anastomotic site. The other 18 rats survived up to the time of planned harvest. Macroscopically, there were adhesions between the SIS graft and the surrounding tissue, and the lumen of the graft was filled with some mucous materials at 2 weeks. By 24 weeks, the regenerated bowel had no adhesion to the surrounding tissue, but some fibrous scar tissue surrounding its external surface was present in all ani- mals. There was no evidence of obstruction or stenosis at Fig 1. Isolated ileal loop with interposed SIS graft before double the anastomotic site, and the lumen was patent with some ileostomy. mucous materials. Diameter of the regenerated bowel 1598 WANG, WATANABE, AND TOKI Table 1.
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