Advertisement
Cardiothoracic| Volume 128, ISSUE 1, P87-97, September 2005

Download started.

Ok

Esophageal Reconstruction with ECM and Muscle Tissue in a Dog Model

      An in vivo study was conducted to determine if an extracellular matrix (ECM) scaffold co-localized with autologous muscle tissue could achieve constructive remodeling of esophageal tissue without stricture. ECM derived from the porcine urinary bladder was processed, decellularized, configured into a tube shape, and terminally sterilized for use as a bioscaffold for esophageal reconstruction in a dog model. Twenty-two dogs were divided into four groups, three groups of five and one group of seven. Groups 1 and 2 were repaired with either ECM alone or muscle tissue alone, respectively. Groups 3 and 4 were repaired with ECM plus either a partial (30%) covering with muscle tissue or a complete (100%) covering with muscle tissue, respectively. Animals in groups 1 and 2 were sacrificed within approximately 3 weeks because of the formation of intractable esophageal stricture. Four of five dogs in group 3 and six of seven dogs in group 4 were survived for 26 days to 230 days and showed constructive remodeling of esophageal tissue with the formation of well organized esophageal tissue layers, minimal stricture, esophageal motility, and a normal clinical outcome. Mechanical testing of a subset of the remodeled esophageal tissue from animals in groups 3 and 4 showed progressive remodeling from a relatively stiff, non-compliant ECM tube structure toward a tissue with near normal biomechanical properties. We conclude that ECM bioscaffolds plus autologous muscle tissue, but not ECM scaffolds or muscle tissue alone, can facilitate the in situ reconstitution of structurally and functionally acceptable esophageal tissue.

      Key Words

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Journal of Surgical Research
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Heitmiller R.F.
        • Fischer A.
        • Liddicoat J.R.
        Cervical esophagogastric anastomosis.
        Dis. Esophagus. 1999; 12: 264
        • Iannettoni M.D.
        • Whyte R.I.
        • Orringer M.B.
        Catastrophic complications of the cervical esophagogastric anastomosis.
        J. Thorac. Cardiovasc. Surg. 1995; 110 (discussion 1500): 1493
        • Luketich J.D.
        • Nguyen N.T.
        • Weigel T.
        • et al.
        Minimally invasive approach to esophagectomy.
        JSLS. 1998; 2: 243
        • Orringer M.B.
        • Marshall B.
        • Iannettoni M.D.
        Transhiatal esophagectomy for treatment of benign and malignant esophageal disease.
        World J. Surg. 2001; 25: 196
        • Yildirim S.
        • Koksal H.
        • Celayir F.
        • et al.
        Colonic interposition vs. gastric pull-up after total esophagectomy.
        J. Gastrointest. Surg. 2004; 8: 675
        • Alcantara P.S.
        • Spencer-Netto F.A.
        • Silva-Junior J.F.
        • et al.
        Gastro-esophageal isoperistaltic bypass in the palliation of irresectable thoracic esophageal cancer.
        Int. Surg. 1997; 82: 249
        • Ellis Jr., F.H.
        Standard resection for cancer of the esophagus and cardia.
        Surg. Oncol. Clin. North. Am. 1999; 8: 279
        • Gawad K.A.
        • Hosch S.B.
        • Bumann D.
        • et al.
        How important is the route of reconstruction after esophagectomy.
        Am. J. Gastroenterol. 1999; 94: 1490
        • Rizk N.P.
        • Bach P.B.
        • Schrag D.
        • et al.
        The impact of complications on outcomes after resection for esophageal and gastroesophageal junction carcinoma.
        J. Am. Coll. Surg. 2004; 198: 42
        • Fujimaki M.
        My devise for the operation of esophageal and gastric cancer.
        Nippon Geka Gakkai Zasshi. 1997; 98 (in Japanese English abstract): 786
        • Inoue H.
        Endoscopic mucosal resection for esophageal and gastric mucosal cancers.
        Can. J. Gastroenterol. 1998; 12: 355
        • Mayoral W.
        The esophacoil stent for malignant esophageal obstruction.
        Gastrointest. Encosc. Clin. North Am. 1999; 9: 423
        • Watson A.
        Self-expanding metal oesophgeal endoprosthesis.
        Eur. J. Gastroenterol. Hepatol. 1998; 10: 363
        • Fitzgerald R.
        Barrett metaplasia.
        Curr. Opin. Oncol. 2004; 16: 372
        • Murray L.
        • Watson P.
        • Johnston B.
        • et al.
        Risk of adenocarcinoma in Barrett’s oesophagus.
        BMJ. 2003; 327: 534
        • Shaheen N.J.
        • Crosby M.A.
        • Bozymski E.M.
        • Sandler R.S.
        Is there publication bias in the reporting of cancer risk in Barrett’s esophagus?.
        Gastroenterology. 2000; 119: 333
        • Powell J.
        • McConkey C.C.
        • Gillison E.W.
        • Spychal R.T.
        Continuing rising trend in oesophageal adenocarcinoma.
        Int. J. Cancer. 2002; 102: 422
        • Overholt B.F.
        • Panjehpour M.
        • Halberg D.L.
        Photodynamic therapy for Barrett’s esophagus with dysplasia and/or early stage carcinoma.
        Gastrointest. Endosc. 2003; 58: 183
        • Pacifico R.J.
        • Wang K.K.
        Nonsurgical management of Barrett’s esophagus with high-grade dysplasia.
        Surg. Oncol. Clin. North Am. 2002; 11: 321
        • Buttar N.S.
        • Wang K.K.
        • Lutzke L.S.
        • et al.
        Combined endoscopic mucosal resection and photodynamic therapy for esophageal neoplasia within Barrett’s esophagus.
        Gastrointest. Endosc. 2001; 54: 682
        • Wolfsen H.C.
        • Hemminger L.L.
        • Raimondo M.
        • Woodward T.A.
        Photodynamic therapy and endoscopic mucosal resection for Barrett’s dysplasia and early esophageal adenocarcinoma.
        South Med. J. 2004; 97: 827
        • Giovannini M.
        • Bories E.
        • Pesenti C.
        • et al.
        Circumferential endoscopic mucosal resection in Barrett’s esophagus with high-grade intraepithelial neoplasia or mucosal cancer. Preliminary results in 21 patients.
        Endoscopy. 2004; 36: 782
        • Katada C.
        • Muto M.
        • Manabe T.
        • et al.
        Esophageal stenosis after endoscopic mucosal resection of superficial esophageal lesions.
        Gastrointest. Endosc. 2003; 57: 165
        • Fitzgerald R.C.
        Ablative mucosectomy is the procedure of choice to prevent Barrett’s cancer.
        Gut. 2003; 52: 16
        • Luman W.
        • Lessels A.M.
        • Palmer K.R.
        Failure of Nd-YAG photocoagulation therapy as treatment for Barrett’s oesophagus.
        Eur. J. Gastroenterol. Hepatol. 1996; 8: 627
        • Sharma P.
        • Bhattacharyya A.
        • Garewal H.S.
        • Sampliner R.E.
        Durability of new squamous epithelium after endoscopic reversal of Barrett’s esophagus.
        Gastrointest. Endosc. 1999; 50: 159
        • Hayashi K.
        • Ando N.
        • Ozawa S.
        • et al.
        A neo-esophagus reconstructed by cultured human esophageal epithelial cells, smooth muscle cells, fibroblasts, and collagen.
        Asaio. J. 2004; 50: 261
        • Sato M.
        • Ando N.
        • Ozawa S.
        • et al.
        An artificial esophagus consisting of cultured human esophageal epithelial cells, polyglycolic acid mesh, and collagen.
        Asaio. J. 1994; 40: M389
        • Sato M.
        • Ando N.
        • Ozawa S.
        • et al.
        A hybrid artificial esophagus using cultured human esophageal epithelial cells.
        Asaio. J. 1993; 39: M554
        • Kropp B.P.
        • Eppley B.L.
        • Prevel C.D.
        • et al.
        Experimental assessment of small intestinal submucosa as a bladder wall substitute.
        Urology. 1995; 46: 396
        • Kropp B.P.
        • Rippy M.K.
        • Badylak S.F.
        • et al.
        Regenerative urinary bladder augmentation using small intestinal submucosa.
        J. Urol. 1996; 155: 2098
        • Sievert K.D.
        • Tanagho E.A.
        Organ-specific acellular matrix for reconstruction of the urinary tract.
        World J. Urol. 2000; 18: 19
        • Yoo J.J.
        • Meng J.
        • Oberpenning F.
        • Atala A.
        Bladder augmentation using allogenic bladder submucosa seeded with cells.
        Urology. 1998; 51: 221
        • Sandusky Jr., G.E.
        • Badylak S.F.
        • Morff R.J.
        • et al.
        Histologic findings after in vivo placement of small intestine submucosal vascular grafts and saphenous vein grafts in the carotid artery in dogs.
        Am. J. Pathol. 1992; 140: 317
        • Sandusky G.E.
        • Lantz G.C.
        • Badylak S.F.
        Healing comparison of small intestine submucosa and ePTFE grafts in the canine carotid artery.
        J. Surg. Res. 1995; 58: 415
        • Schoder M.
        • Pavcnik D.
        • Uchida B.T.
        • et al.
        Small intestinal submucosa aneurysm sac embolization for endoleak prevention after abdominal aortic aneurysm endografting.
        J. Vasc. Interv. Radiol. 2004; 15:: 69
        • MacLeod T.M.
        • Sarathchandra P.
        • Williams G.
        • et al.
        Evaluation of a porcine origin acellular dermal matrix and small intestinal submucosa as dermal replacements in preventing secondary skin graft contraction.
        Burns. 2004; 30: 431
        • Prevel C.D.
        • Eppley B.L.
        • Summerlin D.J.
        • et al.
        Small intestinal submucosa.
        Ann. Plast. Surg. 1995; 35: 381
        • Badylak S.F.
        • Tullius R.
        • Kokini K.
        • et al.
        The use of xenogeneic small intestinal submucosa as a biomaterial for Achilles tendon repair in a dog model.
        J. Biomed. Mater. Res. 1995; 29: 977
        • Dejardin L.M.
        • Arnoczky S.P.
        • Ewers B.J.
        • et al.
        Tissue-engineered rotator cuff tendon using porcine small intestinal submucosa. Histologic and mechanical evaluation in dogs.
        Am. J. Sports Med. 2001; 29: 175
        • Badylak S.
        • Meurling S.
        • Chen M.
        • et al.
        Resorbable bioscaffold for esophageal repair in a dog model.
        J. Pediatr. Surg. 2000; 35: 1097
        • Brant A.M.
        • Shah S.S.
        • Rodgers V.G.
        • et al.
        Biomechanics of the arterial wall under simulated flow conditions.
        J. Biomech. 1988; 21: 107
        • Jankowski R.J.
        • Prantil R.L.
        • Fraser M.O.
        • et al.
        Development of an experimental system for the study of urethral biomechanical function.
        Am. J. Physiol. Renal. Physiol. 2004; 286: F225
        • Labadie R.F.
        • Antaki J.F.
        • Williams J.L.
        • et al.
        Pulsatile perfusion system for ex vivo investigation of biochemical pathways in intact vascular tissue.
        Am. J. Physiol. 1996; 270: H760
        • Raghavan M.L.
        • Webster M.W.
        • Vorp D.A.
        Ex vivo biomechanical behavior of abdominal aortic aneurysm.
        Ann. Biomed. Eng. 1996; 24: 573
        • Vorp D.A.
        • Schiro B.J.
        • Ehrlich M.P.
        • et al.
        Effect of aneurysm on the tensile strength and biomechanical behavior of the ascending thoracic aorta.
        Ann. Thorac. Surg. 2003; 75: 1210
        • Atala A.
        Engineering tissues and organs.
        Curr. Opin. Urol. 1999; 9: 517
        • Atala A.
        Creation of bladder tissue in vitro and in vivo. A system for organ replacement.
        Adv. Exp. Med. Biol. 1999; 462: 31
        • Yoo J.J.
        • Atala A.
        Tissue engineering applications in the genitourinary tract system.
        Yonsei. Med. J. 2000; 41: 789
        • Atala A.
        Tissue engineering in urology.
        Curr. Urol. Rep. 2001; 2: 83
        • Kropp B.P.
        • Cheng E.Y.
        • Pope J.Ct.
        • et al.
        Use of small intestinal submucosa for corporal body grafting in cases of severe penile curvature.
        J. Urol. 2002; 168 (discussion 1745): 1742
        • Strange P.S.
        Small intestinal submucosa for laparoscopic repair of large paraesophageal hiatal hernias.
        Surg. Technol. Int. 2003; 11: 141
        • Badylak S.
        • Kokini K.
        • Tullius B.
        • et al.
        Morphologic study of small intestinal submucosa as a body wall repair device.
        J. Surg. Res. 2002; 103: 190
        • Badylak S.
        • Kokini K.
        • Tullius B.
        • Whitson B.
        Strength over time of a resorbable bioscaffold for body wall repair in a dog model.
        J. Surg. Res. 2001; 99: 282
      1. Methods of Tissue Engineering. Academic Press, San Diego2000: 505-514
        • Master V.A.
        • Wei G.
        • Liu W.
        • Baskin L.S.
        Urothlelium facilitates the recruitment and trans-differentiation of fibroblasts into smooth muscle in acellular matrix.
        J. Urol. 2003; 170: 1628
        • Vaught J.D.
        • Kropp B.P.
        • Sawyer B.D.
        • et al.
        Detrusor regeneration in the rat using porcine small intestinal submucosal grafts.
        J. Urol. 1996; 155: 374
        • Chen F.
        • Yoo J.J.
        • Atala A.
        Acellular collagen matrix as a possible “off the shelf” biomaterial for urethral repair.
        Urology. 1999; 54: 407
        • Price R.D.
        • Das-Gupta V.
        • Frame J.D.
        • Navsaria H.A.
        A study to evaluate primary dressings for the application of cultured keratinocytes.
        Br. J. Plast. Surg. 2001; 54: 687
        • Kipshidze N.
        • Dangas G.
        • Tsapenko M.
        • et al.
        Role of the endothelium in modulating neointimal formation.
        J. Am. Coll. Cardiol. 2004; 44: 733
        • Vouyouka A.G.
        • Jiang Y.
        • Basson M.D.
        Pressure alters endothelial effects upon vascular smooth muscle cells by decreasing smooth muscle cell proliferation and increasing smooth muscle cell apoptosis.
        Surgery. 2004; 136: 282
        • Rheinwald J.G.
        • Green H.
        Serial cultivation of strains of human epidermal keratinocytes.
        Cell. 1975; 6: 331
        • Hillegonds D.J.
        • Record R.
        • Rickey F.A.
        • et al.
        Prime lab sample handling and data analysis for accelerator-based biomedical radiocarbon analysis.
        Radiocarbon. 2001; 43: 305
        • Record R.D.
        • Hillegonds D.
        • Simmons C.
        • et al.
        In vivo degradation of 14C-labeled small intestinal submucosa (SIS) when used for urinary bladder repair.
        Biomaterials. 2001; 22: 2653
        • Rickey F.A.
        • Elmore D.
        • Hillegonds D.
        • et al.
        Re-generation of tissue about an animal-based scaffold.
        Nucl. Instr. Meth. Phy. Res. 2000; 172: 904
        • Badylak S.F.
        • Park K.
        • Peppas N.
        • et al.
        Marrow-derived cells populate scaffolds composed of xenogeneic extracellular matrix.
        Exp. Hematol. 2001; 29: 1310
        • Li F.
        • Li W.
        • Johnson S.
        • et al.
        Low-molecular-weight peptides derived from extracellular matrix as chemoattractants for primary endothelial cells.
        Endothelium. 2004; 11: 199