The use of thoracodorsal nerve transfer in restoration of irreparable C5 and C6 spinal nerve lesions

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1 British Journal of Plastic Surgery (2005) 58, The use of thoracodorsal nerve transfer in restoration of irreparable C5 and C6 spinal nerve lesions M.M. Samardzic*, D.M. Grujicic, L.G. Rasulic, B.R. Milicic Institute of Neurosurgery, Clinical Center of Serbia, Visegradska 26, Belgrade, Serbia and Montenegro Received 21 June 2003; accepted 17 December 2003 KEYWORDS Axillary nerve; Brachial plexus injury; Musculocutaneous nerve; Nerve transfer; Thoracodorsal nerve Summary There are only a few reports on the use of thoracodorsal nerve (TDN) transfer to the musculocutaneous or axillary nerves in cases of directly irreparable brachial plexus injuries. In this study, we analysed outcome and time-course of recovery in correlation with recipient nerves and type of nerve transfer (isolated or in combination with other collateral branches) for 27 patients with transfer to the musculocutaneous or axillary nerves. Using this nerve as donor, we obtained useful functional recovery in all 12 cases for the musculocutaneous nerve, and in 14 (93.3%) of 15 nerve transfers for the axillary nerve. Although, we found no significant statistical difference between analysed patients according to the percentage of recoveries and mean values, we established a better quality and shorter time of recovery for the musculocutaneous nerve. According to obtained results, we consider that transfer may be a valuable method in reconstruction after directly irreparable C5 and C6 spinal nerve lesions. Q 2004 The British Association of Plastic Surgeons. Published by Elsevier Ltd. All rights reserved. The type of donor nerve is an important prognostic factor in nerve transfers for directly irreparable brachial plexus lesions. In cases of upper brachial plexus palsy one of the possibilities is the use of the thoracodorsal nerve (TDN) since this remains functional in majority of the C5 C6 lesions. This method of nerve transfer was introduced by Foerster in 1929, as reported by Narakas. 1 He employed the nerves to the latissimus dorsi or subscapular muscles when repairing lesions of the axillary nerve. Thereafter, the TDN transfer has been *Corresponding author. Tel.: þ ; fax: þ address: gruj@infosky.net reported rarely and with limited number of cases. 1 4 We used this type of nerve transfer to upper arm nerves during last 20 years. 5,6 The purpose of this study is to elucidate characteristics and to determine the value of the TDN transfer through an analysis of our surgical results. Patients and methods Patient population In this study, we analysed a series of 27 patients S /$ - see front matter Q 2004 The British Association of Plastic Surgeons. Published by Elsevier Ltd. All rights reserved. doi: /j.bjps

2 542 M.M. Samardzic et al. with upper brachial plexus palsy due to traction injuries who were operated on since January The age of these patients ranged from 9 to 46 years (mean 27.4 years), with 21 patients (77.7%) aged up to 40 years. In all cases, the supraspinatus, deltoid, and biceps muscles were paralysed. Using clinical, electrodiagnostic (electromyography of the proximal arm and cervical paraspinal muscles, and somatosensory evoked potentials for the musculocutaneous, radial, and median nerves) and radiological (cervical myelography, computed tomography-myelography and magnetic resonance imaging) tests, we diagnosed a variety of injury patterns to the C5, C6 and sometimes C7 spinal nerve roots or spinal nerves. Indications for nerve transfer included preoperatively documented avulsion of the C5 and/or C6 spinal roots or intraoperatively demonstrated peripheral spinal nerve injuries, for which we were not able to determine the severity of structural changes in the proximal spinal nerve stumps precisely. Surgical procedures were done between 2 and 12 months after the injuries and 25 (91.4%) patients were operated within 6 months after injuries. Surgery The extent of surgical exploration was adapted to the reliability of preoperative diagnosis, as we described previously. 5 The functional status of donor and recipient nerves was evaluated using direct electrical nerve stimulation. The choice of the recipient nerve for the TDN transfer was based predominantly on the possibility for direct nerve anastomosis with this nerve or with the other donors. For these 27 patients, we performed 12 reinnervations of the musculocutaneous and 15 reinnervations of the axillary nerve using the TDN as donor. These procedures were in all cases a part of complex brachial plexus reconstruction that included other types of nerve transfer (medial pectoral, intercostal, spinal accessory nerves) or nerve grafting (Table 1). In nine nerve transfers, we combined the thoracodorsal with intercostal, long thoracic or subscapular nerves. The main reason for combined nerve transfer was completion of the suture line in cases with recipient nerves of considerably larger diameter. Microsurgical procedure The TDN was usually joined directly to the recipient nerves in 26 patients. In one case with an extensive peripheral lesion to the musculocutaneous nerve, we used an 8 cm long nerve graft. The neurorrhaphies were performed using standard microsurgical procedure (Fig. 1). The epifascicular epineurium of the recipient nerves was removed in order to reduce their diameter and any fibrosis on the suture line. The sutures were introduced through the epineurium of the TDN and through interfascicular tissue or perineurium of some fascicles of the recipient nerves. Individual anastomoses were completed with two sutures on the upper side of the nerve or with a circumferential suture using four to five stitches around the nerve. In some cases the suturing technique was combined with fibrin glue. Grading of surgical results The results of the TDN transfer were analysed using modification of the grading system which we used in our previous report 5 as follows: (1) Bad denotes no movement or weightless movement. (2) Fair denotes movement against gravity with the ability to hold position, active abduction up to 458, and full range elbow flexion up to 908. (3) Good denotes movement against resistance with ability to repeat movements in succession, active abduction over 458, and full range elbow flexion. (4) Excellent denotes near normal function. Fair, good and excellent results were considered to represent recovery. The quality of recovery was estimated according to the relation between excellent and good vs. fair results. The follow-up period was at least 2 years. Table 1 Summary of 27 nerve transfers using thoracodorsal nerve as donor Donor nerve Recipient nerve Total Musculocutaneous Axillary Thoracodorsal Thoracodorsal and intercostal Thoracodorsal and subscapular or long thoracic 2 3 a 5 Total a One case combined with long thoracic nerve.

3 The use of thoracodorsal nerve transfer in restoration of irreparable C5 and C6 spinal nerve lesions 543 Figure 1 Nerve transfer of the thoracodorsal (TDN) to the axillary nerve (Ax) (white arrow). Note additional anastomosis between the medial pectoral (PM) and musculocutaneous (Mc) nerves (black arrow). Statistical analysis Statistical analysis was done using commercially available software (SPSS 8.0). The following tests were performed: (1) descriptives (number and percentage of cases, mean, minimum and maximum values, standard deviation), (2) Fisher s Exact Test, and (3) T Test. The dependent variables were elbow flexion and arm abduction. The significance of the association of independent variables including a type of nerve transfer (isolated or in combination with other donors), age of the patient, and timing of surgery was tested. A probability value equal to or less than 0.05 was considered significant. recovery was somewhat better in these cases in comparison to the solitary transfers but the number of cases is too small for valid interpretation (Figs. 2 and 3). The first signs of recovery appeared after 4 12 months with the mean of (6.89 ^ 2.26) months for the musculocutaneous, and after 4 13 months with the mean of (7.77 ^ 2.95) for the axillary nerve. The recovery was completed in a period of months with the mean of (13.44 ^ 5.08) months for the musculocutaneous nerve, and 9 24 months with the mean of (17.15 ^ 4.83) months for the axillary nerve. There were neither clinical nor electromyographical signs of recovery for the supraspinatus muscle. Comparative statistical analysis using Fisher s test showed no significant correlation between the age of patients, timing of surgery, recipient nerves, type of nerve transfer (solitary or in combination with other donors) and appearance of initial signs of recovery or final outcome. Discussion Restoration of upper arm function that includes elbow flexion and arm abduction as first priorities presents a major goal in nerve repair of brachial plexus injuries, especially in nerve transfers for Results Useful functional recovery was obtained in all 12 (100%) nerve transfers for the musculocutaneous nerve and in 14 (93.3%) of 15 nerve transfers for the axillary nerve. The extent of recovery was obviously better for the musculocutaneous nerve with 91.6% vs. 57.1% of excellent and good results among recoveries (Table 2). Using solitary nerve transfer of the TDN, we obtained useful recovery in all cases for both nerves. The corresponding rate indicating quality of recovery was better for the musculocutaneous nerve, 87.5% vs. 50% for the axillary nerve. In combined use of donors, we obtained useful recovery in all four nerve transfers for the musculocutaneous nerve and in 4 (80%) of five nerve transfers for the axillary nerve. The quality of Figure 2 Return of strong, full range elbow flexion for a 42-year-old male patient achieved two years after reinnervation of the left musculocutaneous nerve using thoracodorsal nerve transfer.

4 544 M.M. Samardzic et al. Table 2 Results of 27 nerve transfers using thoracodorsal nerve as donor Donor nerve Outcomes (no. of cases) Musculocutaneous nerve Axillary nerve Total Bad Fair Good Excellent Bad Fair Good Excellent Bad Fair Good Excellent Thoracodorsal Thoracodorsal and intercostal Thoracodorsal subscapular or long thoracic a 1 4 Total a One case combined with long thoracic nerve. directly irreparable nerve lesions. In cases of upper brachial plexus palsy, nerve transfers can be done using some collateral branches of the brachial plexus including the TDN. The TDN is a motor nerve that originates from the posterior cord and receives nerve fibers from the seventh, eighth, and sometimes sixth cervical nerves. This nerve has cerebral centers integrated into the function of the upper extremity and innervates the latissimus dorsi muscle. The mean surgically useable length of the TDN is 12.3 cm with a range of cm, and the diameter of the nerve ranges from 2.1 to 3 mm. 6,7 The number of myelinated fibers ranges from 1530 to According to these characteristics, the TDN may be considered as an excellent donor in motor nerve transfers. Generally, the TDN is suitable for motor nerve transfer for several reasons: (1) this is a voluntary muscular nerve with an autonomous function; (2) there is a close functional relationship with upper arm nerves including better cortical reintegration owing to efficient central plasticity based on preexisting cortical and medullary synaptic connections such as in the intraplexal, long thoracic or medial pectoral nerve transfers; 8 (3) there is Figure 3 Near normal function of the left deltoid muscle for a 19-year-old man 10 months after surgery. Reinnervation of the axillary nerve was done using the thoracodorsal nerve. sufficient length for tension-free direct coaptation with the musculocutaneous or axillary nerves in almost all cases, and (4) there are significant number of motor nerve fibers such as in the intraplexal, medial pectoral, spinal accessory, phrenic, and contralateral C7 nerve transfers. 1,5 Generally, the quality of motor recovery depends on a number of motor axons reinnervating the target muscle. The number of motor axons in the TDN is sufficient for reinnervation of the biceps and brachialis muscles through the main musculocutaneous nerve trunk without a need for neurolysis and exclusion 4,9 or redirection of the lateral antebrachial cutaneous nerve sensory fibers. 10 Similarly, we think that there is no need for augmentation by an additional nerve transfer to the brachial muscle branch, although this may be reasonable for other types of nerve transfer as proposed by Tung et al. 9 However, nerve anastomosis should be done distally to the branches to the coracobrachialis since this muscle is not important for elbow flexion and shouldn t be reinnervated. 10 It should be emphasised that in the majority of cases with extended upper brachial plexus palsy involving the C7 spinal nerve, the TDN is not functional and cannot be used for nerve transfer. Regarding functional deficit after the TDN section, we believe that additional palsy of arm adduction and internal rotation due to the loss of the latissimus dorsi are not significant in severely disabled shoulder and arm movement, and present an acceptable sacrifice. 4,5,7 Furthermore, some function of the pectoral muscles may be retained owing to the sparing of some branches of the medial pectoral nerve used in nerve transfer too, and partial preservation of synergic muscles such as the teres major in cases of predominant innervation from the C7 spinal root. 5 The main advantages of this method compared to the intercostal nerve transfer are: there are significantly more motor fibers than in intercostal nerves that contain only motor fibers; 1,5,6 there is no significant axonal mixing; direct

5 The use of thoracodorsal nerve transfer in restoration of irreparable C5 and C6 spinal nerve lesions 545 anastomosis or occasionally anastomosis using short nerve grafts is possible; an anastomosis close to the motor point can be achieved owing to the available length of this nerve, although that is also possible in intercostal nerve transfer but with diminished number of motor fibers; the operation is quicker and less traumatic, 5 and this could be accomplished through the original incision of the infraclavicular approach without a need for separate chest incision. The main disadvantage of spinal accessory nerve transfer compared to this method is the use of 7 20 cm long nerve grafts. 5 Nerve transfer of the TDN is also advantageous to the classical intraplexal nerve transfer using spinal nerve stumps because of their mixed fibre composition, dispersion of regenerating axons with mass innervation, and difficult evaluation of their proximal continuity and structural changes since up to 80% of nerve fibers may be degenerated and fibrous changes expressed. 11 Similarly to the first report by Foerester, Narakas recommended the TDN transfer exclusively for the axillary nerve. 1 However, having in mind its close functional relationship with other upper arm nerves, we also used this nerve in nerve transfer to the musculocutaneous as several other authors did. 2 5 We obtained functional recovery in all 12 cases for the musculocutaneous nerve and in 14 (93.3%) of 15 for the axillary nerve. Our results are supported by those published by Richardson, 3 who obtained the functional recovery of the biceps muscle using the TDN as a donor in four cases with nerve repair delayed for two years, Novak et al., 4 who reported successful reinnervation of the biceps muscle in all six cases, and M4 or M5 grades of elbow flexion in five of them; and Dai et al. 2 who obtained recovery in one case of nerve transfer to the musculocutaneous nerve and in two cases of the nerve transfer to the axillary nerve. On the contrary, Narakas, one of the leading authors in this field used this nerve for reinnervation of the axillary nerve in two cases, without significant functional improvement. 1 He obtained proper reinnervation of the deltoid muscle but not with muscle contractions in arm adduction and internal rotation. Results of the TDN transfer to the axillary nerve are less impressive, especially regarding the quality of recovery, probably due to the functional complexity of the shoulder abduction, the role of the supraspinatus muscle that is not reinnervated in our cases, and essentially antagonistic function of the latissimus dorsi although this could also be successfully retrained. 4 In nine cases, we combined the TDN with other donor nerves, similarly to Narakas, who reported combined use of the spinal accessory nerve and motor branches of the cervical plexus for reinnervation of the suprascapular nerve and, the hypoglossal and accessory nerves for the musculocutaneous nerve, 1 in cases of disproportion of diameters. In these patients, we obtained somewhat higher rate and better quality of functional recovery. According to the results obtained, TDN transfer may be considered as a reliable procedure, especially in restoration of elbow flexion if done during the first year after injury, although successful transfers were also reported in delayed cases. In our opinion, this procedure is likely to be superior to the latissimus dorsi muscle transfer in restoration of elbow flexion because of the preservation of the original biceps tendon and muscle fibers tension and orientation, 9,10 minimal target muscle dissection and consecutive formation of adhesions, 9 simplicity and a significant gain in operative time. As stated previously, using TDN transfers we achieved functionally useful recovery of elbow flexion in all cases, and there was only one possible failure among reported cases (M 2 grade). 4 In comparison to the reported results of the latissimus dorsi muscle transfer, 12,13 aside a higher rate of useful functional recovery, obtained average ranges of elbow flexion and maximum muscle strenghts are at least somewhat higher in TDN transfers. Although the results of TDN transfers to the axillary nerve are less impressive, the same statements are valid for the latissimus dorsi muscle transfer in restoration of arm abduction and external rotation. This is especially true if we bear in mind the possibility of additional nerve transfer to the suprascapular nerve. References 1. Narakas A. Neurotization in the treatment of brachial plexus injuries. In: Gelberman RH, editor. Operative nerve repair and reconstruction. Philadelphia: JB Lippincott Company; p Dai SY, Lin DX, Han Z, Zhong SZ. Transference of thoracodorsal nerve to musculocutaneous or axillary nerve in old traumatic injury. J Hand Surg (Am) 1990;15: Richardson PM. Recovery of biceps function after delayed repair for brachial plexus injury. J Trauma 1997;42: Novak CB, Mackinnon SE, Tung THH. Patient outcome following a thoracodorsal to musculocutaneous nerve transfer for reconstruction of elbow flexion. Br J Plast Surg 2002;55: Samardzic M, Rasulic L, Grujicic D, Milicic B. Results of nerve transfers to the musculocutaneous and axillary nerves. Neurosurgery 2000;46: Samardzic M, Antunovic V, Joksimovic M, Bacetic D. Donor nerves in the reinnervation of brachial plexus. Neurol Res 1986;8: Bartlett SP, May JW, Yaremchuk MJ. The latissimus dorsi

6 546 M.M. Samardzic et al. muscle: a fresh cadaver study of the primary neurovascular pedicle. Plast Reconstr Surg 1981;67: Malessy M, Thomeer R, VanDijk JG. Changing central nervous system control following intercostal nerve transfer. J Neurosurg 1998;89: Tung TH, Novak CB, Mackinnon SE. Nerve transfers to the biceps and brachialis branches to improve elbow flexion strenght after brachial plexus injuries. J Neurosurg 2003;98: Brandt KE, Mackinnon SE. A technique for maximizing biceps recovery in brachial plexus reconstruction. J Hand Surg (Am) 1993;18: Narakas A. Les neurotizations ou transferts nerveux dans les lesions du plexus brachial. Ann Chir Main 1982;1: Krakauer JD, Wood MB. Adult injuries and salvage. In: Peimer CA, editor. Surgery of the hand and upper extremity. New York: McGraw/Hill; p Chen WS. Restoration of elbow flexion by latissimus dorsi myocutaneous or mucle flap. Arch Orthop Trauma Surg 1990;109: