DOI QR코드

DOI QR Code

Rat Peripheral Nerve Regeneration Using Nerve Guidance Channel by Porcine Small Intestinal Submucosa

  • Yi, Jin-Seok (Department of Neurosurgery, Daejeon St. Mary's Hospital, College of Medicine, The Catholic University of Korea) ;
  • Lee, Hyung-Jin (Department of Neurosurgery, Daejeon St. Mary's Hospital, College of Medicine, The Catholic University of Korea) ;
  • Lee, Hong-Jae (Department of Neurosurgery, Daejeon St. Mary's Hospital, College of Medicine, The Catholic University of Korea) ;
  • Lee, Il-Woo (Department of Neurosurgery, Daejeon St. Mary's Hospital, College of Medicine, The Catholic University of Korea) ;
  • Yang, Ji-Ho (Department of Neurosurgery, Daejeon St. Mary's Hospital, College of Medicine, The Catholic University of Korea)
  • Received : 2012.08.24
  • Accepted : 2013.02.04
  • Published : 2013.02.28

Abstract

Objective : In order to develop a novel nerve guidance channel using porcine small intestinal submucosa (SIS) for nerve regeneration, we investigated the possibility of SIS, a tissue consisting of acellular collagen material without cellular immunogenicity, and containing many kinds of growth factors, as a natural material with a new bioactive functionality. Methods : Left sciatic nerves were cut 5 mm in length, in 14 Sprague-Dawley rats. Grafts between the cut nerve ends were performed with a silicone tube (Silicon group, n=7) and rolled porcine SIS (SIS group, n=7). All rats underwent a motor function test and an electromyography (EMG) study on 4 and 10 weeks after grafting. After last EMG studies, the grafts, including proximal and distal nerve segments, were retrieved for histological analysis. Results : Foot ulcers, due to hypesthesia, were fewer in SIS group than in Silicon group. The run time tests for motor function study were 2.67 seconds in Silicon group and 5.92 seconds in SIS group. Rats in SIS group showed a better EMG response for distal motor latency and amplitude than in Silicon group. Histologically, all grafts contained some axons and myelination. However, the number of axons and the degree of myelination were significantly higher in SIS group than Silicon group. Conclusion : These results show that the porcine SIS was an excellent option as a natural biomaterial for peripheral nerve regeneration since this material contains many kinds of nerve growth factors. Furthermore, it could be used as a biocompatible barrier covering neural tissue.

Keywords

References

  1. Badylak SF, Tullius R, Kokini K, Shelbourne KD, Klootwyk T, Voytik SL, et al. : The use of xenogeneic small intestinal submucosa as a biomaterial for Achilles tendon repair in a dog model. J Biomed Mater Res 29 : 977-985, 1995 https://doi.org/10.1002/jbm.820290809
  2. Bejjani GK, Zabramski J; Durasis Study Group : Safety and efficacy of the porcine small intestinal submucosa dural substitute : results of a prospective multicenter study and literature review. J Neurosurg 106 : 1028-1033, 2007 https://doi.org/10.3171/jns.2007.106.6.1028
  3. Borkenhagen M, Stoll RC, Neuenschwander P, Suter UW, Aebischer P : In vivo performance of a new biodegradable polyester urethane system used as a nerve guidance channel. Biomaterials 19 : 2155-2165, 1998 https://doi.org/10.1016/S0142-9612(98)00122-7
  4. Caione P, Boldrini R, Salerno A, Nappo SG : Bladder augmentation using acellular collagen biomatrix : a pilot experience in exstrophic patients. Pediatr Surg Int 28 : 421-428, 2012 https://doi.org/10.1007/s00383-012-3063-0
  5. Danielsen N, Kerns JM, Holmquist B, Zhao Q, Lundborg G, Kanje M : Predegeneration enhances regeneration into acellular nerve grafts. Brain Res 681 : 105-108, 1995 https://doi.org/10.1016/0006-8993(95)00300-F
  6. den Dunnen WF, van der Lei B, Robinson PH, Holwerda A, Pennings AJ, Schakenraad JM : Biological performance of a degradable poly(lactic acid-epsilon-caprolactone) nerve guide : influence of tube dimensions. J Biomed Mater Res 29 : 757-766, 1995 https://doi.org/10.1002/jbm.820290612
  7. Den Dunnen WF, Van der Lei B, Schakenraad JM, Blaauw EH, Stokroos I, Pennings AJ, et al. : Long-term evaluation of nerve regeneration in a biodegradable nerve guide. Microsurgery 14 : 508-515, 1993 https://doi.org/10.1002/micr.1920140808
  8. Favaro G, Bortolami MC, Cereser S, Doná M, Pastorello A, Callegaro L, et al. : Peripheral nerve regeneration through a novel bioresorbable nerve guide. ASAIO Trans 36 : M291-M294, 1990
  9. Geoffrion R, Murphy M, Robert M, Birch C, Ross S, Tang S, et al. : Vaginal paravaginal repair with porcine small intestine submucosa : midterm outcomes. Female Pelvic Med Reconstr Surg 17 : 174-179, 2011 https://doi.org/10.1097/SPV.0b013e31821e5dcf
  10. Gilbert TW, Stewart-Akers AM, Simmons-Byrd A, Badylak SF : Degradation and remodeling of small intestinal submucosa in canine Achilles tendon repair. J Bone Joint Surg Am 89 : 621-630, 2007 https://doi.org/10.2106/JBJS.E.00742
  11. Hadlock T, Elisseeff J, Langer R, Vacanti J, Cheney M : A tissue-engineered conduit for peripheral nerve repair. Arch Otolaryngol Head Neck Surg 124 : 1081-1086, 1998 https://doi.org/10.1001/archotol.124.10.1081
  12. Hadlock T, Sundback C, Hunter D, Cheney M, Vacanti JP : A polymer foam conduit seeded with Schwann cells promotes guided peripheral nerve regeneration. Tissue Eng 6 : 119-127, 2000 https://doi.org/10.1089/107632700320748
  13. Hadlock T, Sundback C, Koka R, Hunter D, Cheney M, Vacanti J : A novel, biodegradable polymer conduit delivers neurotrophins and promotes nerve regeneration. Laryngoscope 109 : 1412-1416, 1999 https://doi.org/10.1097/00005537-199909000-00010
  14. Heath CA, Rutkowski GE : The development of bioartificial nerve grafts for peripheral-nerve regeneration. Trends Biotechnol 16 : 163-168, 1998 https://doi.org/10.1016/S0167-7799(97)01165-7
  15. Henry EW, Chiu TH, Nyilas E, Brushart TM, Dikkes P, Sidman RL : Nerve regeneration through biodegradable polyester tubes. Exp Neurol 90 : 652-676, 1985 https://doi.org/10.1016/0014-4886(85)90162-1
  16. Kiyotani T, Nakamura T, Shimizu Y, Endo K : Experimental study of nerve regeneration in a biodegradable tube made from collagen and polyglycolic acid. ASAIO J 41 : M657-M661, 1995 https://doi.org/10.1097/00002480-199507000-00092
  17. Kiyotani T, Teramachi M, Takimoto Y, Nakamura T, Shimizu Y, Endo K, et al. : Nerve regeneration across a 25-mm gap bridged by a polyglycolic acid-collagen tube : a histological and electrophysiological evaluation of regenerated nerves. Brain Res 740 : 66-74, 1996 https://doi.org/10.1016/S0006-8993(96)00848-7
  18. Kropp BP, Rippy MK, Badylak SF, Adams MC, Keating MA, Rink RC, et al. : Regenerative urinary bladder augmentation using small intestinal submucosa : urodynamic and histopathologic assessment in long-term canine bladder augmentations. J Urol 155 : 2098-2104, 1996 https://doi.org/10.1016/S0022-5347(01)66117-2
  19. Liu Z, Tang R, Zhou Z, Song Z, Wang H, Gu Y : Comparison of two porcine-derived materials for repairing abdominal wall defects in rats. PLoS One 6 : e20520, 2011 https://doi.org/10.1371/journal.pone.0020520
  20. Lundborg G, Kanje M : Bioartificial nerve grafts. A prototype. Scand J Plast Reconstr Surg Hand Surg 30 : 105-110, 1996 https://doi.org/10.3109/02844319609056391
  21. Maquet V, Martin D, Malgrange B, Franzen R, Schoenen J, Moonen G, et al. : Peripheral nerve regeneration using bioresorbable macroporous polylactide scaffolds. J Biomed Mater Res 52 : 639-651, 2000 https://doi.org/10.1002/1097-4636(20001215)52:4<639::AID-JBM8>3.0.CO;2-G
  22. Owen K, Wilshaw SP, Homer-Vanniasinkam S, Bojar RA, Berry H, Ingham E : Assessment of the antimicrobial activity of acellular vascular grafts. Eur J Vasc Endovasc Surg 43 : 573-581, 2012 https://doi.org/10.1016/j.ejvs.2012.01.027
  23. Roeder R, Wolfe J, Lianakis N, Hinson T, Geddes LA, Obermiller J : Compliance, elastic modulus, and burst pressure of small-intestine submucosa (SIS), small-diameter vascular grafts. J Biomed Mater Res 47 : 65-70, 1999 https://doi.org/10.1002/(SICI)1097-4636(199910)47:1<65::AID-JBM9>3.0.CO;2-F
  24. Sacks MS, Gloeckner DC : Quantification of the fiber architecture and biaxial mechanical behavior of porcine intestinal submucosa. J Biomed Mater Res 46 : 1-10, 1999 https://doi.org/10.1002/(SICI)1097-4636(199907)46:1<1::AID-JBM1>3.0.CO;2-7
  25. Tu DD, Seth A, Gil ES, Kaplan DL, Mauney JR, Estrada CR Jr : Evaluation of biomaterials for bladder augmentation using cystometric analyses in various rodent models. J Vis Exp, 2012 in press
  26. Utley DS, Lewin SL, Cheng ET, Verity AN, Sierra D, Terris DJ : Brain-derived neurotrophic factor and collagen tubulization enhance functional recovery after peripheral nerve transection and repair. Arch Otolaryngol Head Neck Surg 122 : 407-413, 1996 https://doi.org/10.1001/archotol.1996.01890160047009
  27. Voytik-Harbin SL, Brightman AO, Kraine MR, Waisner B, Badylak SF : Identification of extractable growth factors from small intestinal submucosa. J Cell Biochem 67 : 478-491, 1997 https://doi.org/10.1002/(SICI)1097-4644(19971215)67:4<478::AID-JCB6>3.0.CO;2-P
  28. Wang X, Li J, Zhang H, Zhang Y : Evaluation of the small intestinal submucosa covered stent in preventing restenosis after percutaneous transluminal angioplasty in the swine. Eur J Radiol 81 : e281-e287, 2012 https://doi.org/10.1016/j.ejrad.2011.06.011
  29. Young RC, Wiberg M, Terenghi G : Poly-3-hydroxybutyrate (PHB) : a resorbable conduit for long-gap repair in peripheral nerves. Br J Plast Surg 55 : 235-240, 2002 https://doi.org/10.1054/bjps.2002.3798
  30. Zhao Q, Lundborg G, Danielsen N, Bjursten LM, Dahlin LB : Nerve regeneration in a 'pseudo-nerve' graft created in a silicone tube. Brain Res 769 : 125-134, 1997 https://doi.org/10.1016/S0006-8993(97)00620-3

Cited by

  1. Approaches to Peripheral Nerve Repair: Generations of Biomaterial Conduits Yielding to Replacing Autologous Nerve Grafts in Craniomaxillofacial Surgery vol.2016, pp.None, 2013, https://doi.org/10.1155/2016/3856262
  2. Influencing Factors Analysis of Facial Nerve Function after the Microsurgical Resection of Acoustic Neuroma vol.60, pp.2, 2013, https://doi.org/10.3340/jkns.2013.0407.001
  3. Can a Small Intestine Segment Be an Alternative Biological Conduit for Peripheral Nerve Regeneration? vol.34, pp.3, 2013, https://doi.org/10.4274/balkanmedj.2015.1601
  4. Biomimetic neural scaffolds: a crucial step towards optimal peripheral nerve regeneration vol.6, pp.6, 2018, https://doi.org/10.1039/c8bm00260f
  5. Peripheral nerve injury and axonotmesis: State of the art and recent advances vol.5, pp.1, 2013, https://doi.org/10.1080/2331205x.2018.1466404
  6. Semitransparent bandages based on chitosan and extracellular matrix for photochemical tissue bonding vol.17, pp.None, 2013, https://doi.org/10.1186/s12938-018-0444-1
  7. Small intestinal submucosa: superiority, limitations and solutions, and its potential to address bottlenecks in tissue repair vol.7, pp.33, 2019, https://doi.org/10.1039/c9tb00530g
  8. Evaluation of postoperative outcomes in patients following multi-level surgical reconstructions with the use Avive soft tissue membrane on nerve after traumatic injury of the upper e vol.9, pp.None, 2013, https://doi.org/10.1177/20503121211023356