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Tunica Repair with Acellular Bladder Matrix Maintains Corporal Tissue Function

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Tunica Repair with Acellular Bladder Matrix Maintains Corporal Tissue Function International Journal of Impotence Research (2007) 19, 602–609 & 2007 Nature Publishing Group All rights reserved 0955-9930/07 $30.00 www.nature.com/ijir ORIGINAL ARTICLE Tunica repair with acellular bladder matrix maintains corporal tissue function D Eberli, R Susaeta, JJ Yoo and A Atala Department of Urology and Wake Forest Institute for Regenerative Medicine, Wake Forest University Health Sciences, Winston-Salem, NC, USA Penile conditions, such as Peyronie’s disease or tumor resection may require surgical reconstruc- tion of the tunica albuginea. Various materials have been proposed, as a biomaterial for tunica albuginea repair, however, little functional data are available. We examined the applicability and functional outcome of a collagen-based matrix derived from the bladder (acellular bladder matrix (ABM)), as a biomaterial for tunica repair. Biocompatibility testing was performed on the matrix, which included mitochondrial metabolic activity, cell viability and apoptosis. Approximately 50% of the dorsal penile tunica albuginea was replaced with the collagen-based matrix patch after surgical removal in 24 New Zealand White rabbits. Cavernosometry and cavernosography were performed. The animals were killed 1, 2 and 3 months after surgery for analyses. The matrix showed excellent biocompatibility. All animals implanted with the matrix survived without any noticeable untoward effects. There was no evidence of inflammation or infection at the time of retrieval. Cavernosometry of the implanted animals demonstrated normal intracavernosal pressures with visual erections. Cavernosography of the repaired corpora showed a normal anatomical configuration. Biomechanical analysis of the retrieved matrices demonstrated similar tensile strengths as native tunica. Histologically, there was only a minimal inflammatory response, which gradually decreased over time. These results show that ABM is biocompatible, durable and effective when used as a tunica substitute. The matrix may be useful as an off-the-shelf biomaterial for patients requiring tunica albuginea repair. International Journal of Impotence Research (2007) 19, 602–609; doi:10.1038/sj.ijir.3901587; published online 2 August 2007 Keywords: penile reconstruction; tunica albuginea; acellular bladder matrix Introduction However, some of these materials have been asso- ciated with donor site morbidity, extensive inflam- Penile conditions, such as Peyronie’s disease, mation resulting in fibrosis and erectile dysfunction fibrosis, tumor resection or augmentation surgery, due to venous leak.1,4,5 often require reconstruction of the tunica albuginea. An ideal biomaterial for tunica repair should be Surgical reconstruction of these conditions has been biocompatible, elicit minimal inflammation, pro- a challenge due to the limited availability of tissues mote new tissue formation, and be able to withstand suitable for tunica albuginea replacement. A variety adequate tensile forces for maintaining structural of materials has been investigated over the years, integrity.6 Acellular bladder matrix (ABM) is a which include the skin, muscular aponeurosis, collagen-based biomaterial processed from the blad- tunica vaginalis, human dura mater, pericardium, der submucosa, known as the lamina propria. The polyethylene, temporalis fascia-free graft, vein patch matrix has shown to be biocompatible, is processed graft, fascia lata graft, Dacron and Goretex.1–3 easily, and has good characteristics for tissue handling. This matrix has been used experimentally and clinically for several applications, including urethra and bladder reconstruction procedures.7–9 Correspondence: Dr A Atala, Wake Forest University In this study, we investigated whether ABM School of Medicine, Medical Center Boulevard, Winston- Salem, NC 27157 USA. possesses the ideal material characteristics required E-mail: [email protected] for penile reconstruction. We examined the applic- Received 13 February 2007; revised 11 May 2007; ability and functional outcome of ABM for tunica accepted 3 June 2007; published online 2 August 2007 repair. Tunica repair with ABM maintains corporal tissue function D Eberli et al 603 Materials and methods MTT (mitochondrial metabolic activity) The mitochondrial metabolic activity of the bioma- Study design terial was determined by the MTT (3-(4,5-di- Acellular bladder matrices, processed from porcine methylthiazol-2-yl)-2,5-diphenyltetrazolium bromide) bladders, were examined for biocompatibility using assay using the direct contact method.13 The cell mitochondrial metabolic activity, cell viability and layers were rinsed with PBS, and 125 mlofMTT apoptosis assays. The matrix was tested in 24 New (Sigma, Saint Louis, MI, USA, 1 mg/ml MTT in PBS Zealand White rabbits weighing approximately containing 1 g/l glucose) was added to each well. 3.5 kg (Millbrook Farms, Concord, MA, USA). After After a 3-h incubation period at 371C, the MTT performing functional assessments, the animals solution was removed, and the insoluble Formazan were killed after 1, 2 and 3 months. The tissue crystals formed were dissolved using 100 mlof samples were retrieved and analyzed histologically, dimethylsulfoxide (Sigma). The absorbance was ultrastructurally and biomechanically. The findings measured at 540 nm using a 96-well plate spectro- were compared to normal controls (four animals). photometer (ELX 800, BioTek Inc., Winooski, VN, USA). The intensity of the blue color is directly proportional to the metabolic activity of the cells and inversely proportional to the toxicity of the material. Preparation of the ABM Porcine bladders, obtained from IBP Inc. (Logan- sport, IN, USA), were processed at ACell, Inc. (West Lafayette, IN, USA). Briefly, each bladder was rinsed Cell viability assays (Neutral Red) with running tap water, and placed in a À201C The cytotoxic and bioactive effects of the biomater- freezer overnight. The bladder was opened and the ial in direct contact with the cells were tested with 14 muscle layer was excised with sharp scissors. The Neutral Red according to the reported standards. remaining tissue, consisting of the lamina propria or The cell layers were rinsed with PBS, and 100 mlof often referred as the bladder submucosa, was placed Neutral Red Solution (Sigma, 0.005% in culture in 0.9% normal saline. The bladders were disin- medium) was added into each well. After a 3-h fected in a solution consisting of peracetic acid, incubation at 371C, the Neutral Red solution was alcohol, and water for 2 h followed by repeated removed, and dye extraction was performed by cycles of sterile phosphate-buffered saline (PBS) adding 100 ml of 1% acetic acid in 50% ethanol water rinses. solution into each well. After placing the wells on a Cells within the ABM were removed using the cell platform shaker for 5 min, the absorbance was lyses technique described previously.10 Briefly, measured at 540 nm by using a 96-well plate bladder lamina propria was treated with distilled spectrophotometer. The intensity of the red color is water in a stirring flask at 41C for 1 day to lyse the directly proportional to the viability of the cells and cells in the tissue. Subsequently, the tissues were inversely proportional to the toxicity of the material. treated with 1% Triton X100 and 0.1% ammonium hydroxide in a stirring flask at 41C for 14 days. The collagen matrix was then rinsed with distilled water Apoptosis index at 41C for 2 days followed by a treatment with PBS The quantification of apoptosis was measured with for 24 h. The bladder matrix was lyophilized, an in situ detection of DNA fragmentation in the cell trimmed to size, packaged, E-beam sterilized stored cultures using a commercially available kit (Titer in a desiccator until use. TACSs, Trevigen, Helgermann, MD, USA) accord- ing to the manufacturer’s instructions. Apoptosis was assessed after 3 days of cell-material contact Biomaterials testing using 96-well plates. No media change was per- Biocompatibility of the ABM was assessed using the formed. Unlabeled cells indicated the level of previously described methods, which include direct background labeling, and TACS-nuclease generated contact cell viability assay, mitochondrial metabolic DNA breaks served as a positive control. The results activity assay and quantification of apoptosis (n ¼ 8 were adjusted for cell density in the monolayer to per group per test).11 Primary mouse dermal fibro- take the high toxicity of latex into account. blasts were used for the biocompatibility testing. ABM fragments (0.03 cm2/well) were placed in the center of subconfluent fibroblast monolayers in 96- Anesthesia and surgery well plates, according to the established stan- All experimental procedures were reviewed and dards.12 Cells on plates not exposed to the bioma- approved by the Institutional Animal Care and Use terial served as a positive control and latex Committee, and were performed in compliance with fragments as a negative control. The material-cell the Animal Welfare Act and the Guide for the Care contact was maintained for 3 days at 371C and 5% and Use of Laboratory Animals. The animals were CO2, followed by each assay. sedated with an intramuscular injection of 10 mg/kg International Journal of Impotence Research Tunica repair with ABM maintains corporal tissue function D Eberli et al 604 ketamine and an intravenous injection of 0.5 mg/ filling in both corpora and by determining the kg acepromazine. After an induction with propofol corporal anatomical contour. Special attention was (4–8 mg/kg, IV), the animals were
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