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Isometric contractile function following nerve grafting: A study of graft storage
Dr. Peter J. Evans MD, PhD,
Dr. David C. Awerbuck MD, FRCS(C),
Dr. Susan E. Mackinnon MD, FRCS(C), FACS,
Ms. Judith A. Wade BSc,
Dr. Nancy H. McKee MD, FRCS(C), FACS,
Dr. Peter J. Evans MD, PhD
Department of Surgery, University of Toronto, Toronto, Ontario, Canada
Search for more papers by this authorDr. David C. Awerbuck MD, FRCS(C)
Department of Surgery, University of Toronto, Toronto, Ontario, Canada
Search for more papers by this authorCorresponding Author
Dr. Susan E. Mackinnon MD, FRCS(C), FACS
Department of Surgery, Washington University, St. Louis, Missouri
Division of Plastic Surgery, Suite 17424 East Pavilion, St. Louis, MO 63110Search for more papers by this authorMs. Judith A. Wade BSc
Department of Surgery, University of Toronto, Toronto, Ontario, Canada
Search for more papers by this authorDr. Nancy H. McKee MD, FRCS(C), FACS
Department of Surgery, University of Toronto, Toronto, Ontario, Canada
Search for more papers by this authorDr. Peter J. Evans MD, PhD,
Dr. David C. Awerbuck MD, FRCS(C),
Dr. Susan E. Mackinnon MD, FRCS(C), FACS,
Ms. Judith A. Wade BSc,
Dr. Nancy H. McKee MD, FRCS(C), FACS,
Dr. Peter J. Evans MD, PhD
Department of Surgery, University of Toronto, Toronto, Ontario, Canada
Search for more papers by this authorDr. David C. Awerbuck MD, FRCS(C)
Department of Surgery, University of Toronto, Toronto, Ontario, Canada
Search for more papers by this authorCorresponding Author
Dr. Susan E. Mackinnon MD, FRCS(C), FACS
Department of Surgery, Washington University, St. Louis, Missouri
Division of Plastic Surgery, Suite 17424 East Pavilion, St. Louis, MO 63110Search for more papers by this authorMs. Judith A. Wade BSc
Department of Surgery, University of Toronto, Toronto, Ontario, Canada
Search for more papers by this authorDr. Nancy H. McKee MD, FRCS(C), FACS
Department of Surgery, University of Toronto, Toronto, Ontario, Canada
Search for more papers by this authorAbstract
In order to assess the effects of storage on nerve grafts, the isometric contractile function of the gastrocnemius muscle was assessed 14 months following sciatic nerve autografting in the rat. Three-centimeter sciatic nerve grafts were stored at either 5°C or 22°C for 6 h, 24 h, or 3 weeks in an organ transplant solution. Muscle mass and maximal force in the fresh control graft group returned to 47% and 36% of normal levels, respectively, which was similar to stored grafts. Storage at 5°C was superior to 22°C and there was no decrement in contractile function in grafts stored up to 3 weeks at 5°C. These findings suggest that the storage of nerve grafts is a feasible technique that might be applied to nerve allografts, thus permitting elective reconstruction of large peripheral nerve gaps. © 1994 John Wiley & Sons, Inc.
References
- 1 Anderson PN, Mitchell J, Mayor D, Stauber VV: An ultrastructural study of the early stages of axonal regeneration through rat nerve grafts. Neuropathol Appl Neurobiol 1983; 9: 455–466.
- 2 Ansselin AD, Pollard JD: Immunopathological factors in peripheral nerve allograft rejection: quantification of lymphocyte invasion and major histocompatibility complex expression. J Neurol Sci 1990; 96: 75–88.
- 3 Ariano MA, Armstrong RB, Edgerton VR: Hindlimb muscle fiber populations of five mammals. J Histochem Cytochem 1973; 21: 51–55.
- 4 Armati PJ, Pollard JD, Gatenby P: Rat and human Schwann cells in vitro can synthesize and express MHC molecules. Muscle Nerve 1990; 113: 106–116.
- 5 Armstrong RB, Phelps RO: Muscle fibre type composition of the rat hindlimb. Am J Anat 1984; 171: 259–272.
- 6 Bain JR, Mackinnon SE, Hudson AR, Falk RE, Falk JA, Hunter DA: The peripheral nerve allograft: an assessment of regeneration across nerve allografts in rats immunosuppressed with cyclosporin. A. Plast Reconstr Surg 1988; 82: 1052–1066.
- 7 Bain JR, Mackinnon SE, Hudson AR, Wade JA, Evans PJ, Makino AP, Hunter DA: The peripheral nerve allograft in the primate immunosuppressed with cyclosporin A. Part 1: Histological and electrophysiological assessment. Plast Reconstr Surg 1992; 90: 1036–1046.
- 8 Bain JR, Mackinnon SE, Hunter DA: Functional evaluation of complete sciatic, peroneal, and posterior tibial nerve lesions in the rat. Plast Reconstr Surg 1989; 83: 129–138.
- 9 Bolesta MJ, Garrett WE, Ribbech BM, Glisson RR, Seaber AV, Goldner JL: Immediate and delayed neurorrhaphy in a rabbit model: a functional, histologic, and biochemical comparison. J Hand Surg 1988; 13A: 352–357.
- 10 Brown CJ, Evans PJ, Mackinnon SE, Bain JR, Makino AP, Hunter DA, Hare G: Interand intraobserver realibility of walking-track analysis to assess sciatic nerve function rats. Microsurgery 1991; 12: 76–79.
- 11 Brown CJ, Mackinnon SE, Evans PJ, Bain JR, Makino AP, Hunter DA, Hare GMT: Self-evaluation of walking track measurement using a sciatic function index. Microsurgery 1989; 10: 226–235.
- 12 Bryan DJ, Miller RA, Costas PD, Wang K-K, Seckel BR: Immunochemistry of skeletal muscle basal lamina grafts in nerve regeneration. Plast Reconstr Surg 1993; 92: 927–940.
- 13 Bucko CD, Steinmuller D: Reinnervation after orthotopic grafting of peripheral nerve segments in inbred rats. Plast Reconstr Surg 1974; 53: 326–331.
- 14 Chung PKC, Chung SKY: Evaluation of Imuran and Locke's solution in peripheral nerve homografts. Exp Neurol 1974; 42: 141–145.
- 15 Dellon AL, Mackinnon SE: Selection of the appropriate parameter to measure Neurol regeneration. Ann Plast Surg 1989; 23: 197–202.
- 16 Edgar D, Timpi R, Theonen H: The heparin-binding domain of laminin is responsible for its effects on neurite outgrowth and neuronal survival. EMBO J 1984; 3: 14631468.
- 17 Evans PJ, Awerbuck DC, Mackinnon SE, Hudson AR, McKee NH: Preservation of peripheral nerve grafts. Surg Forum 1990: 41: 522–524.
- 18 Evans PJ, Bain JR, Mackinnon SE, Makino AP, Hunter DA: Selective reinnervation: a comparison of recovery following microsuture and conduit nerve repair. Brain Res 1991; 559: 315–321.
- 19 Evans PJ, Midha R, Mackinnon SE: The peripheral nerve allograft: a comprehensive review of regeneration and neuroimmunology. Prog Neurobiol (in press).
- 20 Fish JS, Bain JR, McKee NH, Mackinnon SE: Recovery of contractile function in nerve allografted, cyclosporin A-treated primates. Surg Forum 1989; 40: 600–602.
- 21 Fish JS, Bain JR, McKee NH, Mackinnon SE, Hudson AR, Wade JA, Makino AP, Hunter DA: The peripheral nerve allograft in the primate immunosuppressed with cyclosporin A. Part II. Functional evaluation of reinnervated muscle. Plast Reconstr Surg 1992; 90: 1047–1052.
- 22 Frey M, Gruber H, Holle J, Freilinger G: An experimental comparison of the different kinds of muscle reinnervation: nerve suture, nerve implantation, and muscular neurotization. Plast Reconstr Surg 1982; 69: 656–667.
- 23 Gillespie MJ, Gordon T, Murphy PR: Reinnervation of the lateral gastrocnemius and soleus muscles in the rat by their common nerve. J Physiol (Lond) 1986; 372: 485–500.
- 24 Gordon T, Stein RB: Time course and extent of recovery in reinncrvated motor units of cat triceps surae muscles. J Physiol 1982; 323: 307–323.
- 25 Gordon T, Stein RB, Thomas CK: Organization of motor units following cross-reinnervation of antagonistic muscles in the cat hind limb. J Physiol 1986; 374: 443–456.
- 26 Gulati AK: Evaluation of acellular and cellular nerve grafts in repair of rat peripheral nerve. J Neurosurg 1988; 68: 117–123.
- 27 Gulati AK, Cole GP: Nerve graft immunogenecity as a factor determining axonal regeneration in the rat. J Neurosurg 1990; 72: 114–122.
- 28 Gulati AK, Zaiewski AA: Basement membrane component changes in nerve allografts and isografts. Muscle Nerve 1985; 8: 280–283.
- 29 Gutmann E, Melichna J, Syrovy I: Contraction properties and ATPase activity in fast and slow muscle of the rat during denervation. Exp Nenrol 1972; 36: 488–497.
- 30 Gutmann E, Sanders FK: Functional recovery following nerve grafts and other types of nerve bridge. Brain 1942; 65: 373–407.
- 31 Gutmann E, Sanders FK: Recovery of fibre numbers and diameters in the regeneration of peripheral nerves. J Physiol (Lond) 1943; 101: 489–518.
- 32 Hall SM: The effect of inhibiting Schwann cell mitosis on the re-innervation of acellular autografts in the peripheral nervous system of the mouse. Neuropathol Appl Neurobiol 1986; 12: 401–414.
- 33 Hall SM: Regeneration in cellular and acellular autografts in the peripheral nervous system. Neuropathol Appl Neurobiol 1986; 12: 27–46.
- 34 Hare GMT, Evans PJ, Mackinnon SE, Best TJ, Midha R, Szalai JP, Hunter DA: Walking track analysis: utilization of individual footprint parameters. Ann Plast Surg 1993; 30: 147–153.
- 35 Hare GMT, Evans PJ, Mackinnon SE, Hunter DA, Best TJ: Walking track analysis: a long-term assessment of peripheral nerve recovery. Plast Reconstr Surg 1992; 89: 251–258.
- 36 Hausamen JE: A comparative study of autologous and homologous nerve grafts in rabbits, In 6th International Congress of Plastic and Reconstructive Surgery. Paris, Masson, 1975, pp 24–29.
- 37 Huber C: Repair of peripheral nerve injuries. Surg Gynecol Obstet 1920; 30: 464–471.
- 38 Huber GC: Transplantation of peripheral nerves. Arch Neurol Psychiatry (Chicago) 1919; 2: 466–480.
- 39 Ide C: Nerve regeneration and Schwann call basal lamina: observations of the long-term regeneration. Arch Histol Jpn 1983; 46: 243–257.
- 40 Ide C, Osawa T, Tohkyama K: Nerve regeneration through allogeneic nerve grafts, with special reference to Schwann cell basal lamina. Prog Neurobiol 1990; 34: 1–38.
- 41 Ide C, Tohkyama K, Yokota R, Nitatori T, Onodera S: Schwann cell basal lamina and nerve regeneration. Brain Res 1983; 288: 61–75.
- 42 Jabaley ME, Burns JE, Orcutt BS, Bryant WM: Comparison of histologic and functional recovery after peripheral nerve repair. J Hand Surg 1976; 1: 119–130.
- 43 Kerns JM, Fakhouri AJ, Pavkovic IM: A twitch tension method to assess motor nerve function in the rat. J Neurosci Meth 1987; 19: 259–266.
- 44 Kleinman HK, Sephel GC, Tashiro K, Weeks BS, Burrous BA, Adler SH, Yamada Y, Martin GA: Laminin in neuronal development. Ann NY Acad Sci 1990; 580: 302–310.
- 45 Levi ADO, Evans PJ, Mackinnon SE, Bunge RP: Cold storage of peripheral nerves: an in vitro assay of cell viability and function. Glia 1994; 10: 121–131.
- 46 Lewis HP, McLaurin RL: Application of tissue transplant technique to experimental nerve grafting. J Trauma 1969; 9: 227–235.
- 47 Mackinnon SE, Dellon AL; Surgery of the Peripheral Nerve. New York, Thieme, 1988.
- 48 Mackinnon SE, Dellon AL, O'Brien JP: Changes in nerve fiber numbers distal to a nerve repair in the rat sciatic nerve model. Muscle Nerve 1991; 14; 1116–1122.
- 49 Mackinnon SE, Hudson AR, Falk RE, Kline D, Hunter DA: Peripheral nerve allograft: an assessment of regeneration across pretreated nerve allografts. Neurosurgery 1984; 15: 690–693.
- 50 Mackinnon SE, Hudson AR, Hunter DA: Histologic assessment of nerve regeneration in the rat. Plast Reconstr Surg 1985; 75: 384–388.
- 51 McNamara MJ, Garrett WE, Seaber AV, Goldner JL: Neurorrhaphy, nerve grafting, and neurotization: a functional comparison of nerve reconstruction techniques. J Hand Surg 1987; 12A: 354–360.
- 52 Midha R, Evans PJ, Mackinnon SE, Best TJ, Hare GMT, Hunter DA, Wade JA: Comparison of regeneration across nerve allografts with temporary or continuous Cyclosporin A immunosuppression. J Neurosurg 1992; 78; 90–100.
- 53 Osawa T, Ide C, Tohyama K: Nerve regeneration through allogenic nerve grafts in mice. Arch Histol Jpn 1986; 49: 69–81.
- 54 Pollard JD, McLeod JG: Fresh and predegenerate nerve allografts and isografts in Tremble mice. Muscle Nerve 1981; 4: 274–281.
- 55 Richter HP: Impairment of motor recovery after late nerve suture: experimental study in the rabbit. Part 1: Functional and electromyographic findings. Neurosurgery 1982; 10: 70–74.
- 56 Richter HP, Ketelsen UP: Impairment of motor recovery after late nerve suture: experimental study in the rabbit. Part 2: Morphological findings. Neurosurgery 1982; 10: 75–85.
- 57 Ruwe PA, Trumble TE: A functional evaluation of cryopreserved peripheral nerve autografts. J Reconstr Microsurg 1990; 6: 239–244.
- 58 Singh R, Mechelse K, Stefanko S: Role of tissue typing on preserved nerve allografts in dogs. J Neurol Neurosurg Psychiatry 1977; 40: 865–871.
- 59 Singh R, Vriesendorp HM, Mechelse K, Stefanko S: Nerve allografts and histocompatibility in dogs. J Neurosurg 1977; 47: 737–743.
- 60 Sketelj J, Bresjanac M, Popovic M: Rapid growth of regenerating axons across the segments of sciatic nerve devoid of Schwann cells. J Neurosci Res 1989; 24: 153–162.
- 61 Sunderland S, Capacity of reinnervated muscles to function efficiently after prolonged denervation. Arch Neurol Psychiatry 1950; 64: 755–771.
- 62 Swett JE, Wikholm RP, Torigoc Y, Blanks RHJ: Peripheral nerve repair: relationship between functional recovery and the identities of regenerated motoneurons. Neurosci Abstr 1987; 13: 117. 6.
- 63 Tajima K, Tohyama K, Ide C, Abe M, Morioka I: Regeneration through nerve allografts in the cynomolgous monkey. (Macaca fascicularis). J Bone Joint Surg 1991; 73A: 172–185.
- 64 Thomas CK, Stein RB, Gordon T, Lee RG, Elleker MG: Patterns of reinnervation and motor unit recruitment in human hand muscles after complete ulnar and median nerve section and resuture. J Neurol Neurosurg Psychiatry 1987; 50: 259–268.
- 65 Trumbic TE, Walen JT, Troiano N, Jacobson S: Cryoprotection: Effects on Cultured Schwann Cells and with Cryosurgery. Anahdeim, CA, Orthopaedic Research Society, 1990, p 581.
- 66
Weiss P:
Functional nerve regeneration through frozendried nerve grafts in cats and monkeys.
Soc Exp Biol Med Proc
1943;
54:
277–279.
10.3181/00379727-54-14402P Google Scholar
- 67
Weiss P,
Taylor C:
Repair of peripheral nerves by grafts of frozen-dried nerve.
Soc Exp Biol Med Proc
1943;
52:
326–328.
10.3181/00379727-52-14141P Google Scholar
- 68 Wekerle H, Schwab M, Linington C, Meyermann R: Antigen presentation in the peripheral nervous system: Schwann cells present endogenous myelin autoantigens to lymphocytes. Eur J Immunol 1986; 16: 1551–1557.
- 69 Zaiewski AA, Gulati AK: Evaluation of histocompatibility as a factor in the repair of nerve with a frozen nerve allograft. J Neurosurg 1982; 56: 550–554.
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