Direct cord implantation in brachial plexus avulsions: revised technique using a single stage combined anterior (first) posterior (second) approach and end-to-side side-to-side grafting neurorrhaphy

Sherif M Amr; Ahmad M Essam; Amr MS Abdel-Meguid; Ahmad M Kholeif; Ashraf N Moharram; Rashed ER El-Sadek

doi:10.1186/1749-7221-4-8

Journal of Brachial Plexus and Peripheral Nerve Injury, Table of Contents

J Brachial Plex Peripher Nerve Inj 2009; 04(01): e43-e59
DOI: 10.1186/1749-7221-4-8

Research article

Amr et al; licensee BioMed Central Ltd.

Direct cord implantation in brachial plexus avulsions: revised technique using a single stage combined anterior (first) posterior (second) approach and end-to-side side-to-side grafting neurorrhaphy^[*]

Sherif M Amr

¹The Department of Orthopaedics and Traumatology, Cairo University, Cairo, Egypt

²Hand and Microsurgery Service, Al-Helal Hospital, Cairo, Egypt

,

Ahmad M Essam

¹The Department of Orthopaedics and Traumatology, Cairo University, Cairo, Egypt

,

Amr MS Abdel-Meguid

¹The Department of Orthopaedics and Traumatology, Cairo University, Cairo, Egypt

³Department of Orthopaedics and Traumatology, Beni-Suef Faculty of Medicine, Beni-Suef, Egypt

,

Ahmad M Kholeif

¹The Department of Orthopaedics and Traumatology, Cairo University, Cairo, Egypt

,

Ashraf N Moharram

¹The Department of Orthopaedics and Traumatology, Cairo University, Cairo, Egypt

,

Rashed ER El-Sadek

²Hand and Microsurgery Service, Al-Helal Hospital, Cairo, Egypt

⁴The Department of Orthopaedics and Traumatology, Al-Azhar University, Cairo, Egypt

› Author Affiliations
Subject Editor:

Abstract

Background The superiority of a single stage combined anterior (first) posterior (second) approach and end-to-side side-to-side grafting neurorrhaphy in direct cord implantation was investigated as to providing adequate exposure to both the cervical cord and the brachial plexus, as to causing less tissue damage and as to being more extensible than current surgical approaches.

Methods The front and back of the neck, the front and back of the chest up to the midline and the whole affected upper limb were sterilized while the patient was in the lateral position; the patient was next turned into the supine position, the plexus explored anteriorly and the grafts were placed; the patient was then turned again into the lateral position, and a posterior cervical laminectomy was done. The grafts were retrieved posteriorly and side grafted to the anterior cord. Using this approach, 5 patients suffering from complete traumatic brachial plexus palsy, 4 adults and 1 obstetric case were operated upon and followed up for 2 years. 2 were C5,6 ruptures and C7,8T1 avulsions. 3 were C5,6,7,8T1 avulsions. C5,6 ruptures were grafted and all avulsions were cord implanted.

Results Surgery in complete avulsions led to Grade 4 improvement in shoulder abduction/flexion and elbow flexion. Cocontractions occurred between the lateral deltoid and biceps on active shoulder abduction. No cocontractions occurred after surgery in C5,6 ruptures and C7,8T1 avulsions, muscle power improvement extended into the forearm and hand; pain disappeared.

Limitations include spontaneous recovery despite MRI appearance of avulsions, fallacies in determining intraoperative avulsions (wrong diagnosis, wrong level); small sample size; no controls rule out superiority of this technique versus other direct cord reimplantation techniques or other neurotization procedures; intra- and interobserver variability in testing muscle power and cocontractions.

Conclusion Through providing proper exposure to the brachial plexus and to the cervical cord, the single stage combined anterior (first) and posterior (second) approach might stimulate brachial plexus surgeons to go more for direct cord implantation. In this study, it allowed for placing side grafts along an extensive donor recipient area by end-to-side, side-to-side grafting neurorrhaphy and thus improved results.

Level of evidence Level IV, prospective case series.

Full Text

References

References
1 Frazier CH, Skillern PG. Supraclavicular subcutaneous lesions of the brachial plexus not associated with skeletal injuries. J Am Med Assoc 1911; 57: 1957-1963
2 Bonney G, Jamieson A. Reimplantation of C7 and C8. Communication au symposium sur le plexus brachial. Int Microsurg 1979; 1: 103-106
3 Carlstedt T, Anand P, Hallin R, Misra PV, Norén G, Seferlis T. Spinal nerve root repair and reimplantation of avulsed ventral roots into the spinal cord after brachial plexus injury. J Neurosurg 2000; 93 (2 Suppl) 237-247 11012054
4 Carlstedt T. Root repair review: basic science background and clinical outcome. Restor Neurol Neurosci 2008; 26 (2–3) 225-241 18820413
5 Cajal SR. Degeneration and Regeneration of the nervous system. Hafner; New York: 1928
6 Carlstedt TP, Hallin RG, Cullheim S, Risling M. Reinnervation of hind limb muscles after ventral root avulsion and implantation in the lumbar spinal cord of the adult rat. Acta Physiol Scand 1986; 128: 645-656 10.1111/j.1748-1716.1986.tb08024.x 3811990
7 Carlstedt TP, Linda H, Hedstroem KG, Nilsson-Remahl IA. Functional recovery in primates with brachial plexus injury after spinal cord implantation of avulsed ventral roots. J of Neurology, Neurosurgery, and Psychiatry 1993; 56: 649-654 10.1136/jnnp.56.6.649
8 Carlstedt T, Grane P, Hallin RG, Norén G. Return of function after spinal cord implantation of avulsed spinal nerve roots. Lancet 1995; 346 (8986) 1323-1325 10.1016/S0140-6736(95)92342-X 7475770
9 Carlstedt T, Norén G. Repair of ruptured spinal nerve roots in a brachial plexus lesion. Case report. J Neurosurg 1995; 82 (4) 661-663 7897534
10 Carlstedt T, Anand P, Htut M, Misra P, Svensson M. Restoration of hand function and so called “breathing arm” after intraspinal repair of C5-T1 brachial plexus avulsion injury. Case report. Neurosurg Focus 2004; 16 (5) E7 10.3171/foc.2004.16.5.8 15174827
11 Lin PH, Cheng H, Huang WC, Chuang TY. Spinal cord implantation with acidic fibroblast growth factor as a treatment for root avulsion in obstetric brachial plexus palsy. J Chin Med Assoc 2005; 68 (8) 392-396 16138720
12 Chow BC, Blaser S, Clarke HM. Predictive value of computed tomographic myelography in obstetrical brachial plexus palsy. Plast Reconstr Surg 2000; 106: 971-977 10.1097/00006534-200010000-00001 11039366
13 Hems TE, Birch R, Carlstedt T. The role of magnetic resonance imaging in the management of traction injuries to the adult brachial plexus. J Hand Surg [Br] 1999; 24 (5) 550-555 10597930
14 Terzis JK, Papakonstantinou KC. The surgical treatment of brachial plexus injuries in adults. Plast Reconstr Surg 2000; 106: 1097-1122 10.1097/00006534-200010000-00022 11039383
15 Venkatramani H, Bhardwaj P, Faruquee SR, Sabapathy SR. Functional outcome of nerve transfer for restoration of shoulder and elbow function in upper brachial plexus injury. J Brachial Plex Peripher Nerve Inj 2008; 3: 15 2432056 18505571 10.1186/1749-7221-3-15
16 Millesi H, Meissl G, Berger A. Further experience with interfascicular grafting of the median, ulnar and radial nerves. J Bone Joint Surg Am. 1981; 58 (2) 209-218
17 Arcand MA, Reider B. Shoulder and upper arm. In: Reider B. The orthopaedic physical examination. Elsevier; Philadelphia: 2nd edition 2004: 17-66
18 Tennent TD, Beach WR, Meyers JF. A review of the special tests associated with shoulder examination. Part I: the rotator cuff tests. Am J Sports Med 2003; 31 (1) 154-160 12531773
19 Richards DP, Burkhart SS, Lo IK. Subscapularis tears: arthroscopic repair techniques. Orthop Clin North Am 2003; 34 (4) 485-498 Review 10.1016/S0030-5898(03)00096-8 14984188
20 McFarland EG, Selhi HS, Keyurapan E. Clinical evaluation of impingement: what to do and what works. J Bone Joint Surg Am 2006; 88: 432-441 16475277
21 Amr SM, Moharram AN, Abdel-Meguid KM. Augmentation of partially regenerated nerves by end-to-side side-to-side grafting neurotization: experience based on eight late obstetric brachial plexus cases. J Brachial Plex Peripher Nerve Inj 2006; 1: 6 1764873 17147803 10.1186/1749-7221-1-6
22 Hierner R, Becker M, Berger A. Indications and results of operative treatment in birth-related brachial plexus injuries. Handchir Mikrochir Plast Chir 2005; 37 (5) 323-331 10.1055/s-2005-865898 16287017
23 Narakas AO. Neurotization in the treatment of brachial plexus injuries. In: Gelberman R. Operative Nerve Repair and Reconstruction. Lippincott Williams and Wilkins Company; Philadelphia: 1991
24 Waikakul S, Wongtragul S, Vandurongwan V. Restoration of elbow flexion in brachial plexus avulsion injury-comparing spinal accessory nerve transfer with intercostals nerve transfer. Hand Surg Am. 1999; 24 (3) 571-576 10.1053/jhsu.1999.0571
25 Amr SM. Traumatic brachial plexus palsy; a report of 30 cases. Medical Journal of Cairo University 2000; 68: 715-730
26 Hattori Y, Doi K, Toh S, Baliarsing AS. Surgical approach to the spinal accessory nerve for brachial plexus reconstruction. J Hand Surg [Am] 2001; 26 (6) 1073-1076 10.1053/jhsu.2001.28762 11721253
27 Hentz VR. Microneural reconstruction of the brachial plexus. In: Green DP, Hotchkiss RN. Operative hand surgery. Churchill-Livingstone; New York Edinburgh London Melbourne Tokyo: 1993: 1223-1252
28 Leffert RD. Brachial plexus. In: Green DP, Hotchkiss RN. Operative hand surgery. Churchill-Livingstone; New York Edinburgh London Melbourne Tokyo: 1993: 1483-1516
29 Millesi H. Chirurgie der peripheren Nerven. In: Spezieller Teil, 2. Urban&Schwarzenberg; Plexus brachialis und seine Aeste Muenchen Wien Baltimore: 1992: 79-112
30 Amr SM, Moharram AN. Repair of brachial plexus lesions by end-to-side side-to-side grafting neurorrhaphy: experience based on 11 cases. Microsurgery 2005; 25 (2) 126-146 10.1002/micr.20036 15389968
31 Juergens-Becker A, Penkert G, Samii M. Therapie traumatischer Armplexuslaesionen. Deutsches Aerzteblatt 1996; 93 (Heft 49) C-2275-2279
32 Dubuisson AS, Kline D, Weinshel SS. Posterior subscapular approach to the brachial plexus: report of 102 patients. J Neurosurg 1993; 79: 319-330 10.3171/jns.1993.79.3.0319 8360726
33 Kline DG, Donner TR, Happel L, Smith B, Richter H. 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 1738028
34 Kratimenos GP, Crockard HA. The far lateral approach for ventrally placed foramen magnum and upper cervical spine tumours. Br J Neurosurg. 1993; 7 (2) 129-140 10.3109/02688699309103469 8494614
35 Sen CN, Sekhar LN. An extreme lateral approach to intradural lesions of the cervical spine and foramen magnum. Neurosurgery 1990; 27: 197-204 10.1097/00006123-199008000-00004 2385336
36 Verbiest H. A lateral approach to the cervical spine: technique and indications. J Neurosurg 1968; 28: 191-203 10.3171/jns.1968.28.3.0191 5643912
37 Crockard HA, Rogers M. Open reduction of traumatic atlanto-axial rotatory dislocation with use of the extreme lateral approach: a report of two cases. J Bone Joint Surg Am. 1996; 78 (3) 431-436 8613452
38 Wu JC, Huang WC, Huang MC, Tsai YA, Chen YC, Shih YH, Cheng H. A novel strategy for repairing preganglionic cervical root avulsion in brachial plexus injury by sural nerve grafting. J Neurosurg 2009; 110 (4) 775-785 10.3171/2008.8.JNS08328 19119881
39 Narakas AO. Thoughts on neurotization or nerve transfers in irreparable nerve lesions. In: Terzis JK. Microreconstruction of nerve injuries. WB Saunders; Philadelphia: 1987: 447-454
40 Narakas AO. Thoughts on neurotization or nerve transfers in irreparable nerve lesions. Clinics in Plastic Surgery 1984; 11 (1) 153-159 6705464
41 Yan JG, Matloub HS, Sanger JR, Zhang LL, Riley DA, Jaradeh SS. A modified end-to-side method for peripheral nerve repair: large epineurial window helicoid technique versus small epineurial window standard end-to-side technique. J Hand Surg [Am] 2002; 27 (3) 484-492 10.1053/jhsu.2002.32953 12015724
42 Morgenstern DA, Asher RA, Naidu M, Carlstedt T, Levine JM, Fawcett JW. Expression and glycanation of the NG2 proteoglycan in developing, adult, and damaged peripheral nerve. Mol Cell Neurosci 2003; 24 (3) 787-802 10.1016/S1044-7431(03)00245-8 14664826
43 Amr SM, Abdel-Meguid KMS, Kholeif AM. Allo-and xenotransplantation of vascularized spinal cord segments together with or without the attached plexus of nerves (lumbosacral plexus). A possible solution to spinal cord injuries. A review article. Medical Journal of Cairo University 2000; 68: 239-267
44 Cullheim S, Carlstedt T, Lindå H, Risling M, Ulfhake B. Motoneurons reinnervate skeletal muscle after ventral root implantation into the spinal cord of the cat. Neuroscience 1989; 29 (3) 725-733 10.1016/0306-4522(89)90144-9 2739906
45 Carlstedt T, Cullheim S, Risling M, Ulfhake B. Nerve fibre regeneration across the PNS-CNS interface at the root-spinal cord junction. Brain Res Bull 1989; 22 (1) 93-102 10.1016/0361-9230(89)90133-0 2713720
46 Carlstedt T, Dalsgaard CJ, Molander C. Regrowth of lesioned dorsal root nerve fibers into the spinal cord of neonatal rats. Neurosci Lett 1987; 74 (1) 14-18 10.1016/0304-3940(87)90043-7 3550529
47 Carlstedt T, Lindå H, Cullheim S, Risling M. Reinnervation of hind limb muscles after ventral root avulsion and implantation in the lumbar spinal cord of the adult rat. Acta Physiol Scand 1986; 128 (4) 645-646 10.1111/j.1748-1716.1986.tb08024.x 3811990
48 Carlstedt T. Regenerating axons form nerve terminals at astrocytes. Brain Res 1985; 347 (1) 188-191 10.1016/0006-8993(85)90911-4 2864985
49 Carlstedt T. Regrowth of cholinergic and catecholaminergic neurons along a peripheral and central nervous pathway. Neuroscience 1985; 15 (2) 507-518 10.1016/0306-4522(85)90229-5 4022338
50 Carlstedt T. Dorsal root innervation of spinal cord neurons after dorsal root implantation into the spinal cord of adult rats. Neurosci Lett 1985; 55 (3) 343-348 10.1016/0304-3940(85)90459-8 3839295
51 Carlstedt T. Regrowth of anastomosed ventral root nerve fibers in the dorsal root of rats. Brain Res 1983; 272 (1) 162-165 10.1016/0006-8993(83)90374-8 6616193
52 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 (3–4) 405-414 10.1016/0361-9230(93)90272-D 8457890
53 Cullheim S, Wallquist W, Hammarberg H, Lindå H, Piehl F, Carlstedt T, Risling M. Properties of motoneurons 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 (1–3) 309-316 10.1016/S0165-0173(02)00213-8 12589929
54 Wallquist W, Patarroyo M, Thams S, Carlstedt T, Stark B, Cullheim S, Hammarberg H. Laminin chains in rat and human peripheral nerve: distribution and regulation during development and after axonal injury. J Comp Neurol 2002; 454 (3) 284-293 10.1002/cne.10434 12442319
55 Carlstedt T. Nerve fibre regeneration across the peripheral-central transitional zone. J Anat 1997; 190 (Pt 1) 51-56 1467583 9034881 10.1046/j.1469-7580.1997.19010051.x
56 Cullheim S, Carlstedt T, Risling M. Axon regeneration of spinal motoneurons following a lesion at the cord-ventral root interface. Spinal Cord 1999; 37 (12) 811-819 10.1038/sj.sc.3100916 10602523
57 Li Y, Yamamoto M, Raisman G, Choi D, Carlstedt T. An experimental model of ventral root repair showing the beneficial effect of transplanting olfactory ensheathing cells. Neurosurgery 2007; 60 (4) 734-740 10.1227/01.NEU.0000255406.76645.EA 17415211
58 Li Y, Carlstedt T, Berthold CH, Raisman G. Interaction of transplanted olfactory-ensheathing cells and host astrocytic processes provides a bridge for axons to regenerate across the dorsal root entry zone. Exp Neurol 2004; 188 (2) 300-308 10.1016/j.expneurol.2004.04.021 15246830
59 Bär KJ, Saldanha GJ, Kennedy AJ, Facer P, Birch R, Carlstedt T, Anand P. GDNF and its receptor component Ret in injured human nerves and dorsal root ganglia. Neuroreport 1998; 9 (1) 43-47 9592045
60 Blits B, Dijkhuizen PA, Carlstedt TP, Poldervaart H, Schiemanck S, Boer GJ, Verhaagen J. Adenoviral vector-mediated expression of a foreign gene in peripheral nerve tissue bridges implanted in the injured peripheral and central nervous system. Exp Neurol 1999; 160 (1) 256-267 10.1006/exnr.1999.7204 10630210
61 Hendriks WT, Eggers R, Carlstedt TP, Zaldumbide A, Tannemaat MR, Fallaux FJ, Hoeben RC, Boer GJ, Verhaagen J. Lentiviral vector-mediated reporter gene expression in avulsed spinal ventral root is short-term, but is prolonged using an immune “stealth” transgene. Restor Neurol Neurosci 2007; 25 (5–6) 585-599 18418947
62 Eggers R, Hendriks WT, Tannemaat MR, van Heerikhuize JJ, Pool CW, Carlstedt TP, Zaldumbide A, Hoeben RC, Boer GJ, Verhaagen J. Neuroregenerative effects of lentiviral vector-mediated GDNF expression in reimplanted ventral roots. Mol Cell Neurosci 2008; 39 (1) 105-117 Epub 2008 Jun 7. 10.1016/j.mcn.2008.05.018 18585464
63 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 (2) 303-316 10.1016/j.expneurol.2004.05.014 15380481
64 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 (3) 304-310 10.1007/s002210050627 9989436
65 Carlstedt TP, Hallin RG, Hedström KG, Nilsson-Remahl IA. Functional recovery in primates with brachial plexus injury after spinal cord implantation of avulsed ventral roots. J Neurol Neurosurg Psychiatry 1993; 56 (6) 649-654 489615 8509779 10.1136/jnnp.56.6.649
66 Carlstedt T. Functional recovery after ventral root avulsion and implantation in the spinal cord. Clin Neurol Neurosurg 1993; 95 (Suppl) S109-111 10.1016/0303-8467(93)90046-J 8467587
67 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 (3–4) 447-451 10.1016/0361-9230(93)90277-I 8457894
68 Htut M, Misra VP, Anand P, Birch R, Carlstedt T. Motor recovery and the breathing arm after brachial plexus surgical repairs, including re-implantation of avulsed spinal roots into the spinal cord. J Hand Surg Eur Vol 2007; 32 (2) 170-178 10.1016/j.jhsb.2006.11.011 17224225
69 Htut M, Misra P, Anand P, Birch R, Carlstedt T. Pain phenomena and sensory recovery following brachial plexus avulsion injury and surgical repairs. J Hand Surg [Br] 2006; 31 (6) 596-605 Epub 2006 Jul 5. 16822598
70 Kato N, Htut M, Taggart M, Carlstedt T, Birch R. The effects of operative delay on the relief of neuropathic pain after injury to the brachial plexus: a review of 148 cases. J Bone Joint Surg Br 2006; 88 (6) 756-759 10.1302/0301-620X.88B6.16995 16720769
71 Frostick SP, Yin Q, Kemp G. Schwann cells, neurotrophic factors, and peripheral nerve regeneration. Microsurgery 1998; 18: 397-405 10.1002/(SICI)1098-2752(1998)18:7<397::AID-MICR2>3.0.CO;2-F 9880154
72 Mackay-Sim A, Feron F, Cochrane J, Bassingthwaighte L, Bayliss C, Davies W, Fronek P, Gray C, Kerr G, Licina P, Nowitzke A, Perry C, Silburn PAS, Urquhart S, Geraghty T. Autologous olfactory ensheathing cell transplantation in human paraplegia: a 3-year clinical trial. Brain 2008; 131: 2376-2386 2525447 18689435 10.1093/brain/awn173

Supplementary Material

Additional file 1 The pre- and postoperative motor power grades of the individual muscles in each patient. Table 2 representing the pre- and postoperative motor power grades of the individual muscles in each patient

Direct cord implantation in brachial plexus avulsions: revised technique using a single stage combined anterior (first) posterior (second) approach and end-to-side side-to-side grafting neurorrhaphy[*]

Direct cord implantation in brachial plexus avulsions: revised technique using a single stage combined anterior (first) posterior (second) approach and end-to-side side-to-side grafting neurorrhaphy^[*]