Skip to main content
Top
Published in: BMC Surgery 1/2013

Open Access 01-12-2013 | Research article

Ventral root re-implantation is better than peripheral nerve transplantation for motoneuron survival and regeneration after spinal root avulsion injury

Authors: Huanxing Su, Qiuju Yuan, Dajiang Qin, Xiaoying Yang, Wai-Man Wong, Kwok-Fai So, Wutian Wu

Published in: BMC Surgery | Issue 1/2013

Login to get access

Abstract

Background

Peripheral nerve (PN) transplantation and ventral root implantation are the two common types of recovery operations to restore the connection between motoneurons and their target muscles after brachial plexus injury. Despite experience accumulated over the past decade, fundamental knowledge is still lacking concerning the efficacy of the two microsurgical interventions.

Methods

Thirty-eight adult female Sprague–Dawley rats were divided into 5 groups. Immediately following root avulsion, animals in the first group (n = 8) and the second group (n = 8) received PN graft and ventral root implantation respectively. The third group (n = 8) and the fourth group (n = 8) received PN graft and ventral root implantation respectively at one week after root avulsion. The fifth group received root avulsion only as control (n = 6). The survival and axonal regeneration of severed motoneurons were investigated at 6 weeks post-implantation.

Results

Re-implantation of ventral roots, both immediately after root avulsion and in delay, significantly increased the survival and regeneration of motoneurons in the avulsed segment of the spinal cord as compared with PN graft transplantation.

Conclusions

The ventral root re-implantation is a better surgical repairing procedure than PN graft transplantation for brachial plexus injury because of its easier manipulation for re-implanting avulsed ventral roots to the preferred site, less possibility of causing additional damage and better effects on motoneuron survival and axonal regeneration.
Appendix
Available only for authorised users
Literature
1.
go back to reference Holtzer CA, Marani E, Lakke EA, Thomeer RT: Repair of ventral root avulsions of the brachial plexus: a review. J Peripher Nerv Syst. 2002, 7: 233-242. 10.1046/j.1529-8027.2002.02031.x.CrossRefPubMed Holtzer CA, Marani E, Lakke EA, Thomeer RT: Repair of ventral root avulsions of the brachial plexus: a review. J Peripher Nerv Syst. 2002, 7: 233-242. 10.1046/j.1529-8027.2002.02031.x.CrossRefPubMed
2.
go back to reference Bertelli JA, Ghizoni MF: Concepts of nerve regeneration and repair applied to brachial plexus reconstruction. Microsurgery. 2006, 26: 230-244. 10.1002/micr.20234.CrossRefPubMed Bertelli JA, Ghizoni MF: Concepts of nerve regeneration and repair applied to brachial plexus reconstruction. Microsurgery. 2006, 26: 230-244. 10.1002/micr.20234.CrossRefPubMed
3.
go back to reference Risling M, Fried K, Linda H, Carlstedt T, Cullheim S: Regrowth of motor axons following spinal cord lesions. Distribution of laminin and collagen in the CNS scar tissue. Brain Res Bull. 1993, 30: 403-413.CrossRef Risling M, Fried K, Linda H, Carlstedt T, Cullheim S: Regrowth of motor axons following spinal cord lesions. Distribution of laminin and collagen in the CNS scar tissue. Brain Res Bull. 1993, 30: 403-413.CrossRef
4.
go back to reference Remahl S, Angeria M, Remahl IN, Carlstedt T, Risling M: Observations at the CNS-PNS Border of Ventral Roots Connected to a Neuroma. Front Neurol. 2010, 25: 136- Remahl S, Angeria M, Remahl IN, Carlstedt T, Risling M: Observations at the CNS-PNS Border of Ventral Roots Connected to a Neuroma. Front Neurol. 2010, 25: 136-
5.
go back to reference Bertelli JA, Mira JC: Brachial plexus repair by peripheral nerve grafts directly into the spinal cord in rats. Behavioral and anatomical evidence of functional recovery. J Neurosurg. 1994, 81: 107-114. 10.3171/jns.1994.81.1.0107.CrossRefPubMed Bertelli JA, Mira JC: Brachial plexus repair by peripheral nerve grafts directly into the spinal cord in rats. Behavioral and anatomical evidence of functional recovery. J Neurosurg. 1994, 81: 107-114. 10.3171/jns.1994.81.1.0107.CrossRefPubMed
6.
go back to reference Wu W, Han K, Li L, Schinco FP: Implantation of PNS graft inhibits the induction of nitric oxide synthase and enhances the survival of spinal motoneurons due to root avulsion. Exp Neurol. 1994, 129: 335-339. 10.1006/exnr.1994.1176.CrossRefPubMed Wu W, Han K, Li L, Schinco FP: Implantation of PNS graft inhibits the induction of nitric oxide synthase and enhances the survival of spinal motoneurons due to root avulsion. Exp Neurol. 1994, 129: 335-339. 10.1006/exnr.1994.1176.CrossRefPubMed
7.
go back to reference Moissonnier P, Reviron T, Ye JH, Horvat JC: Motoneurons of the injured spinal cord of the adult dog can grow lengthy axons into an autologous peripheral nerve graft. A retrograde axonal tracing study. Spinal Cord. 1996, 34: 320-325. 10.1038/sc.1996.59.CrossRefPubMed Moissonnier P, Reviron T, Ye JH, Horvat JC: Motoneurons of the injured spinal cord of the adult dog can grow lengthy axons into an autologous peripheral nerve graft. A retrograde axonal tracing study. Spinal Cord. 1996, 34: 320-325. 10.1038/sc.1996.59.CrossRefPubMed
8.
go back to reference Novikova L, Novikov L, Kellerth JO: Effects of neurotransplants and BDNF on the survival and regeneration of injured adult spinal motoneurons. Eur J Neurosci. 1997, 9: 774-2777.CrossRef Novikova L, Novikov L, Kellerth JO: Effects of neurotransplants and BDNF on the survival and regeneration of injured adult spinal motoneurons. Eur J Neurosci. 1997, 9: 774-2777.CrossRef
9.
go back to reference Rhrich-Haddout F, Kassar-Duchossoy L, Bauchet L, Destombes J, Thiesson D, Butler-Browne G, Lyoussi B, Baillet-Derbin C, Horvat JC: Alpha-motoneurons of the injured cervical spinal cord of the adult rat can reinnervate the biceps brachii muscle by regenerating axons through peripheral nerve bridges: combined ultrastructural and retrograde axonal tracing study. J Neurosci Res. 2001, 64: 476-486. 10.1002/jnr.1099.CrossRefPubMed Rhrich-Haddout F, Kassar-Duchossoy L, Bauchet L, Destombes J, Thiesson D, Butler-Browne G, Lyoussi B, Baillet-Derbin C, Horvat JC: Alpha-motoneurons of the injured cervical spinal cord of the adult rat can reinnervate the biceps brachii muscle by regenerating axons through peripheral nerve bridges: combined ultrastructural and retrograde axonal tracing study. J Neurosci Res. 2001, 64: 476-486. 10.1002/jnr.1099.CrossRefPubMed
10.
go back to reference Holtzer CA, Marani E, van Dijk GJ, Thomeer RT: Repair of ventral root avulsion using autologous nerve grafts in cats. J Peripher Nerv Syst. 2003, 8: 17-22. 10.1046/j.1529-8027.2003.03004.x.CrossRefPubMed Holtzer CA, Marani E, van Dijk GJ, Thomeer RT: Repair of ventral root avulsion using autologous nerve grafts in cats. J Peripher Nerv Syst. 2003, 8: 17-22. 10.1046/j.1529-8027.2003.03004.x.CrossRefPubMed
11.
go back to reference Su HX, Zhang WM, Guo JS, Guo AC, Yuan QJ, Wu W: Neural progenitor cells enhance the survival and axonal regeneration of injured motoneurons after transplantation into the avulsed ventral horn of adult rats. J Neurotrauma. 2009, 26: 67-80. 10.1089/neu.2008.0656.CrossRefPubMed Su HX, Zhang WM, Guo JS, Guo AC, Yuan QJ, Wu W: Neural progenitor cells enhance the survival and axonal regeneration of injured motoneurons after transplantation into the avulsed ventral horn of adult rats. J Neurotrauma. 2009, 26: 67-80. 10.1089/neu.2008.0656.CrossRefPubMed
12.
go back to reference Bertelli JA, Ghizoni MF: Brachial plexus avulsion injury repairs with nerve transfers and nerve grafts directly implanted into the spinal cord yield partial recovery of shoulder and elbow movements. Neurosurgery. 2003, 52: 1385-1389. 10.1227/01.NEU.0000065134.21334.D7.CrossRefPubMed Bertelli JA, Ghizoni MF: Brachial plexus avulsion injury repairs with nerve transfers and nerve grafts directly implanted into the spinal cord yield partial recovery of shoulder and elbow movements. Neurosurgery. 2003, 52: 1385-1389. 10.1227/01.NEU.0000065134.21334.D7.CrossRefPubMed
13.
go back to reference Fournier HD, Menei P, Mercier P: Ideal intraspinal implantation site for the repair of ventral root avulsion after brachial plexus injury in humans. A preliminary anatomical study. Surg Radiol Anat. 2001, 23: 191-195. 10.1007/s00276-001-0191-y.CrossRefPubMed Fournier HD, Menei P, Mercier P: Ideal intraspinal implantation site for the repair of ventral root avulsion after brachial plexus injury in humans. A preliminary anatomical study. Surg Radiol Anat. 2001, 23: 191-195. 10.1007/s00276-001-0191-y.CrossRefPubMed
14.
go back to reference Carlstedt T, Aldskogius H, Hallin RG, Nilsson-Remahl I: Novel surgical strategies to correct neural deficits following experimental spinal nerve root lesions. Brain Res Bull. 1993, 30: 447-451. 10.1016/0361-9230(93)90277-I.CrossRefPubMed Carlstedt T, Aldskogius H, Hallin RG, Nilsson-Remahl I: Novel surgical strategies to correct neural deficits following experimental spinal nerve root lesions. Brain Res Bull. 1993, 30: 447-451. 10.1016/0361-9230(93)90277-I.CrossRefPubMed
15.
go back to reference Hallin RG, Carlstedt T, Nilsson-Remahl I, Risling M: Spinal cord implantation of avulsed ventral roots in primates; correlation between restored motor function and morphology. Exp Brain Res. 1999, 124: 304-310. 10.1007/s002210050627.CrossRefPubMed Hallin RG, Carlstedt T, Nilsson-Remahl I, Risling M: Spinal cord implantation of avulsed ventral roots in primates; correlation between restored motor function and morphology. Exp Brain Res. 1999, 124: 304-310. 10.1007/s002210050627.CrossRefPubMed
16.
go back to reference Carlstedt T, Anand P, Hallin R, Misra PV, Nore¨n G, Seferlis T: Spinal nerve root repair and reimplantation of avulsed ventral roots into the spinal cord after brachial plexus injury. J Neurosurg Spine. 2000, 93: 237-247.CrossRef Carlstedt T, Anand P, Hallin R, Misra PV, Nore¨n G, Seferlis T: Spinal nerve root repair and reimplantation of avulsed ventral roots into the spinal cord after brachial plexus injury. J Neurosurg Spine. 2000, 93: 237-247.CrossRef
17.
go back to reference Blits B, Carlstedt TP, Ruitenberg MJ, de Winter F, Hermens WT, Dijkhuizen PA, Claasens JW, Eggers R, van der Sluis R, Tenenbaum L, Boer GJ, Verhaagen J: Rescue and sprouting of motoneurons following ventral root avulsion and reimplantation combined with intraspinal adeno-associated viral vector-mediated expression of glial cell line-derived neurotrophic factor or brain-derived neurotrophic factor. Exp Neurol. 2004, 189: 303-316. 10.1016/j.expneurol.2004.05.014.CrossRefPubMed Blits B, Carlstedt TP, Ruitenberg MJ, de Winter F, Hermens WT, Dijkhuizen PA, Claasens JW, Eggers R, van der Sluis R, Tenenbaum L, Boer GJ, Verhaagen J: Rescue and sprouting of motoneurons following ventral root avulsion and reimplantation combined with intraspinal adeno-associated viral vector-mediated expression of glial cell line-derived neurotrophic factor or brain-derived neurotrophic factor. Exp Neurol. 2004, 189: 303-316. 10.1016/j.expneurol.2004.05.014.CrossRefPubMed
18.
go back to reference Eggers R, Tannemaat MR, Ehlert EM, Verhaagen J: A spatio-temporal analysis of motoneuron survival, axonal regeneration and neurotrophic factor expression after lumbar ventral root avulsion and implantation. Exp Neurol. 2010, 223: 207-220. 10.1016/j.expneurol.2009.07.021.CrossRefPubMed Eggers R, Tannemaat MR, Ehlert EM, Verhaagen J: A spatio-temporal analysis of motoneuron survival, axonal regeneration and neurotrophic factor expression after lumbar ventral root avulsion and implantation. Exp Neurol. 2010, 223: 207-220. 10.1016/j.expneurol.2009.07.021.CrossRefPubMed
19.
go back to reference Carlstedt T, Havton L: The longitudinal spinal cord injury: Lessons from intraspinal plexus, cauda equina and medullary conus lesions. Handb Clin Neurol. 2012, 109: 337-354.CrossRefPubMed Carlstedt T, Havton L: The longitudinal spinal cord injury: Lessons from intraspinal plexus, cauda equina and medullary conus lesions. Handb Clin Neurol. 2012, 109: 337-354.CrossRefPubMed
20.
go back to reference Chai H, Wu W, So KF, Yip H: Survival and regeneration of motoneurons in adult rats by re-implantation of ventral root following spinal root avulsion. NeuroReport. 2000, 11: 1249-1252. 10.1097/00001756-200004270-00021.CrossRefPubMed Chai H, Wu W, So KF, Yip H: Survival and regeneration of motoneurons in adult rats by re-implantation of ventral root following spinal root avulsion. NeuroReport. 2000, 11: 1249-1252. 10.1097/00001756-200004270-00021.CrossRefPubMed
21.
go back to reference Gu HY, Chai H, Zhang JY, Yao ZB, Zhou LH, Wong WM, Bruce I, Wu W: Survival, regeneration and functional recovery of motoneurons in adult rats by reimplantation of ventral root following spinal root avulsion. Eur J Neurosci. 2004, 19: 2123-2131. 10.1111/j.0953-816X.2004.03295.x.CrossRefPubMed Gu HY, Chai H, Zhang JY, Yao ZB, Zhou LH, Wong WM, Bruce I, Wu W: Survival, regeneration and functional recovery of motoneurons in adult rats by reimplantation of ventral root following spinal root avulsion. Eur J Neurosci. 2004, 19: 2123-2131. 10.1111/j.0953-816X.2004.03295.x.CrossRefPubMed
22.
go back to reference Gu HY, Chai H, Zhang JY, Yao ZB, Zhou LH, Wong WM, Bruce IC, Wu WT: Survival, regeneration and functional recovery of motoneurons after delayed reimplantation of avulsed spinal root in adult rat. Exp Neurol. 2005, 192: 89-99. 10.1016/j.expneurol.2004.10.019.CrossRefPubMed Gu HY, Chai H, Zhang JY, Yao ZB, Zhou LH, Wong WM, Bruce IC, Wu WT: Survival, regeneration and functional recovery of motoneurons after delayed reimplantation of avulsed spinal root in adult rat. Exp Neurol. 2005, 192: 89-99. 10.1016/j.expneurol.2004.10.019.CrossRefPubMed
23.
go back to reference Li L, Wu W, Lin LF, Lei M, Oppenheim RW, Houenou LJ: Rescue of adult mouse motoneurons from injury-induced cell death by a glial cell line-derived neurotrophic factor. Proc Natl Acad Sci USA. 1995, 92: 9771-9775. 10.1073/pnas.92.21.9771.CrossRefPubMedPubMedCentral Li L, Wu W, Lin LF, Lei M, Oppenheim RW, Houenou LJ: Rescue of adult mouse motoneurons from injury-induced cell death by a glial cell line-derived neurotrophic factor. Proc Natl Acad Sci USA. 1995, 92: 9771-9775. 10.1073/pnas.92.21.9771.CrossRefPubMedPubMedCentral
24.
go back to reference Wu W: Potential roles of gene expression change in adult rat spinal motoneurons following axonal injury: a comparison among c-jun, off-affinity nerve growth factor receptor (LNGFR), and nitric oxide synthase (NOS). Exp Neurol. 1996, 141: 190-200. 10.1006/exnr.1996.0153.CrossRefPubMed Wu W: Potential roles of gene expression change in adult rat spinal motoneurons following axonal injury: a comparison among c-jun, off-affinity nerve growth factor receptor (LNGFR), and nitric oxide synthase (NOS). Exp Neurol. 1996, 141: 190-200. 10.1006/exnr.1996.0153.CrossRefPubMed
25.
go back to reference Kline DG, Donner TR, Happel L, Smith B, Richter HP: Intraforaminal repair of plexus spinal nerves by a posterior approach: an experimental study. J Neurosurg. 1992, 76: 459-470. 10.3171/jns.1992.76.3.0459.CrossRefPubMed Kline DG, Donner TR, Happel L, Smith B, Richter HP: Intraforaminal repair of plexus spinal nerves by a posterior approach: an experimental study. J Neurosurg. 1992, 76: 459-470. 10.3171/jns.1992.76.3.0459.CrossRefPubMed
26.
go back to reference Lang EM, Schlegel N, Sendtner M, Asan E: Effects of root replantation and neurotrophic factor treatment on long-term motoneuron survival and axonal regeneration after C7 spinal root avulsion. Exp Neurol. 2005, 194: 341-354. 10.1016/j.expneurol.2005.02.018.CrossRefPubMed Lang EM, Schlegel N, Sendtner M, Asan E: Effects of root replantation and neurotrophic factor treatment on long-term motoneuron survival and axonal regeneration after C7 spinal root avulsion. Exp Neurol. 2005, 194: 341-354. 10.1016/j.expneurol.2005.02.018.CrossRefPubMed
27.
go back to reference Hoffmann CF, Thomeer RT, Marani E: Reimplantation of ventral rootlets into the cervical spinal cord after their avulsion: an anterior surgical approach. Clin Neurol Neurosurg. 1993, 95: S112-S118.CrossRefPubMed Hoffmann CF, Thomeer RT, Marani E: Reimplantation of ventral rootlets into the cervical spinal cord after their avulsion: an anterior surgical approach. Clin Neurol Neurosurg. 1993, 95: S112-S118.CrossRefPubMed
28.
go back to reference Holtzer CA, Dahan A, Verschure PC, van Dijk JG, Marani E, Thomeer RT: Nerve grafting from spinal cord to spinal nerve: a microsurgical technique in cats. J Neurosci Methods. 1996, 70: 163-169. 10.1016/S0165-0270(96)00114-8.CrossRefPubMed Holtzer CA, Dahan A, Verschure PC, van Dijk JG, Marani E, Thomeer RT: Nerve grafting from spinal cord to spinal nerve: a microsurgical technique in cats. J Neurosci Methods. 1996, 70: 163-169. 10.1016/S0165-0270(96)00114-8.CrossRefPubMed
29.
go back to reference Hoffmann CF, Thomeer RT, Marani E: Ventral root avulsions of the cat spinal cord at the brachial plexus level (cervical 7). Eur J Morphol. 1990, 28: 418-429.PubMed Hoffmann CF, Thomeer RT, Marani E: Ventral root avulsions of the cat spinal cord at the brachial plexus level (cervical 7). Eur J Morphol. 1990, 28: 418-429.PubMed
30.
go back to reference Hoffmann CF, Marani E, Gert VD, Kamp W, Thomeer RT: Reinnervation and reimplanted ventral rootlets in the cervical spinal cord of the cat. J Neurosurg. 1996, 8: 234-243.CrossRef Hoffmann CF, Marani E, Gert VD, Kamp W, Thomeer RT: Reinnervation and reimplanted ventral rootlets in the cervical spinal cord of the cat. J Neurosurg. 1996, 8: 234-243.CrossRef
32.
go back to reference Höke A, Redett R, Hameed H, Jari R, Zhou C, Li ZB, Griffin JW, Brushart TM: Schwann cells express motor and sensory phenotypes that regulate axon regeneration. J Neurosci. 2006, 26: 9646-9655. 10.1523/JNEUROSCI.1620-06.2006.CrossRefPubMed Höke A, Redett R, Hameed H, Jari R, Zhou C, Li ZB, Griffin JW, Brushart TM: Schwann cells express motor and sensory phenotypes that regulate axon regeneration. J Neurosci. 2006, 26: 9646-9655. 10.1523/JNEUROSCI.1620-06.2006.CrossRefPubMed
33.
go back to reference Ruigrok TJ, Crowe A, Donkelaar HJ: Dendrite distribution of identified motoneurons in the lumbar spinal cord of the turtle Pseudemys scripta elegans. J Comp Neurol. 1985, 238: 275-285. 10.1002/cne.902380304.CrossRefPubMed Ruigrok TJ, Crowe A, Donkelaar HJ: Dendrite distribution of identified motoneurons in the lumbar spinal cord of the turtle Pseudemys scripta elegans. J Comp Neurol. 1985, 238: 275-285. 10.1002/cne.902380304.CrossRefPubMed
34.
go back to reference Cullheim S, Wallquist W, Hammarberg H, Linda H, Piehl F, Carlstedt T, Risling M: Properties of motoneuros underlying their regenerative capacity after axon lesions in the ventral funiculus or at the surface of the spinal cord. Brain Res. Brain Res Rev. 2002, 40: 309-316. 10.1016/S0165-0173(02)00213-8.CrossRefPubMed Cullheim S, Wallquist W, Hammarberg H, Linda H, Piehl F, Carlstedt T, Risling M: Properties of motoneuros underlying their regenerative capacity after axon lesions in the ventral funiculus or at the surface of the spinal cord. Brain Res. Brain Res Rev. 2002, 40: 309-316. 10.1016/S0165-0173(02)00213-8.CrossRefPubMed
Metadata
Title
Ventral root re-implantation is better than peripheral nerve transplantation for motoneuron survival and regeneration after spinal root avulsion injury
Authors
Huanxing Su
Qiuju Yuan
Dajiang Qin
Xiaoying Yang
Wai-Man Wong
Kwok-Fai So
Wutian Wu
Publication date
01-12-2013
Publisher
BioMed Central
Published in
BMC Surgery / Issue 1/2013
Electronic ISSN: 1471-2482
DOI
https://doi.org/10.1186/1471-2482-13-21

Other articles of this Issue 1/2013

BMC Surgery 1/2013 Go to the issue