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Intrinsic Hand Muscle Reinnervation by Median-Ulnar End-to-Side Bridge Nerve Graft: Case Report
SCIENTIFIC ARTICLE
Intrinsic Hand Muscle Reinnervation by Median-Ulnar End-to-Side Bridge Nerve Graft: Case Report M. Magdi Sherif, MD, Adel H. Amr, MD Recovery of either the motor or sensory functions has not been consistently achieved in upper extremity end-to-side neurorrhaphy; this technique was only indicated when more conventional nerve repair was not possible. In most studies, the whole median or ulnar nerve was used for end-to-side neurotization. In this report, we present 4 cases of high-median or ulnar nerve laceration in which a nerve graft was placed end-to-side between the median and ulnar motor fascicles close to the wrist. At 4 months after surgery, 3 of 4 patients began to recover active movement of the affected small muscles of the hand. EMG and nerve conduction studies confirmed that nerve conduction was through the nerve grafts. (J Hand Surg 2010;35A:446–450. Copyright © 2010 by the American Society for Surgery of the Hand. All rights reserved.) Key words High-median/ulnar nerve injury, double end-to-side nerve graft, bridge graft, hand intrinsic muscles reinnervation.
urrently, the most accepted treatment of peripheral nerve injury is a primary, tension-free repair whenever possible. In high or old median or ulnar nerve lesions, sensory improvement is expected after nerve repair, but intrinsic muscle recovery is rarely satisfactory. Muscle atrophy and fibrosis progress in proportion to the duration of denervation.1 Because the regenerating axons grow at a slow rate, they reach their target end organ after the muscle has atrophied and has become unresponsive to stimuli. A variety of methods have been used to enhance the rate or increase the number of regenerating axons. These include pharmacological agents, external electrical stimulation, implanted electrodes, and transplantation of embryonic motor neurons or sensory ganglion
C
From the Department of Plastic Surgery, Ain Shams University, Cairo, Egypt. The authors are grateful to the anonymous reviewers whose comments significantly helped improve the presentation. Received for publication May 22, 2009; accepted in revised form October 28, 2009. No benefits in any form have been received or will be received related directly or indirectly to the subject of this article. Corresponding author: M. Magdi Sherif, MD, Department of Plastic Surgery, Ain Shams University, 2-A Alsayed abou Shady Street, Heliopolis, Cairo 11361, Egypt; e-mail: magdisherif@ yahoo.com. 0363-5023/10/35A03-0014$36.00/0 doi:10.1016/j.jhsa.2009.10.033
446 䉬 © ASSH 䉬 Published by Elsevier, Inc. All rights reserved.
into the cut nerve. During the past decade, numerous studies have demonstrated the effectiveness of end-toside neurorrhaphy for muscle reinnervation in animal models.2–5 In clinical studies, this technique has been applied successfully to produce temporary innervation of the facial muscles and prevent denervation atrophy until the axons of a cross facial nerve graft reach the paralyzed side of the face.6,7 However, the results of end-to-side median-ulnar neurorrhaphy have not always been successful, with more recovery of the large proximal muscles8 –11 than in the intrinsic hand muscles.10,11 Sensory recovery in the hand after this procedure is also unpredictable; it varies from protective sensation9,12–14 to full recovery,8 even with normal anatomical orientation.11 Therefore, this technique has been recommended only when more conventional repair is not possible.10 In most of the previous studies, the whole injured median or ulnar nerve was used for end-to-side suture to the uninjured nerve.8,9 –11 In one report,10 nerve grafts were used to connect the 2 nerves without respect to the sensory and motor arrangement of the fascicles. Experimentally, it has been shown that axons can also grow through a nerve graft joining 2 adjacent nerves by 2 end-to-side neurorrhaphies with or without deliberate axonotomy of the donor nerve.2–15 This was used clin-
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ically in facial palsy to produce temporary innervation of the facial muscles without affecting the muscles of the donor nerve.6,16,17 To shorten the distance axons have to travel to reach the intrinsic muscles and to prevent their denervation atrophy, we used an end-to-side nerve graft between the intrinsic motor fascicles of the median and ulnar nerves near the wrist in 4 cases of high-median and ulnar nerve laceration. CASE REPORTS Case 1 A 34-year-old man sustained a road traffic accident with deep abrasion of the left forearm, exposing the median nerve at the elbow, which was completely cut. The area was debrided followed by flap coverage of the exposed nerve. After the area completely healed, the infection subsided and the scars softened, and the patient was operated on again. The median nerve was grafted using 4 sural nerve cables, each measuring 6 cm for the innervation of the long flexors and to regain hand sensation. To avoid atrophy of the thenar muscles, we used another graft to bridge the motor branches of the median and ulnar nerves in the palm through 2 additional small incisions located over the expected motor branches of both nerves. In this area, the motor nerve is completely separate from the sensory branches and the regenerating axons will run through the shortest possible distance. An epineural window was performed in each nerve and a single cable 3 cm long was sutured end-to-side with 10-0 suture. At 1.5 months after the surgery, Tinel’s sign of regenerating axons through the bridge graft was noted near the thenar eminence. One month later, there was some recovery in the thenar bulk with weak active abduction and opposition of the thumb. At the 4th postoperative month, the power of these muscles could be graded as M3 to M4 (Fig. 1). EMG and nerve conduction studies done at that time showed some recovery of the flexor carpi radialis after stimulation of the left median nerve at the elbow (no activity at rest and complete interference pattern with average motor units in volition), indicating reinnervation of the flexor muscles. Stimulation of the ulnar nerve at the wrist gave a powerful muscle-evoked response for the abductor pollicis brevis. In contrast, stimulation of the median nerve at the wrist and elbow gave no response at this muscle, indicating its reinnervation through the bridge graft from the motor branch of the ulnar nerve. One year after the surgery, while Tinel’s sign of the regenerating median nerve was still at the wrist level, the patient was able to use his computer normally.
FIGURE 1: Case 1 at 1 year after bridge graft, showing functioning abductor pollicis brevis against resistance.
EMG done at that time showed no response of the abductor pollicis brevis on stimulation of the median nerve; there was also good response on stimulation of the ulnar nerve. Case 2 A 23-year-old man was injured by broken glass at the middle part of the left forearm. The wound was sutured primarily, but the patient noticed weakness of the hand with loss of sensation of the ulnar 1-1/2 fingers. The patient was seen for the first time 6 months after the injury. Examination at that time revealed a complete ulnar nerve injury with wasting of the interosseous muscles and partial clawing of the hand. At surgery, a 5-cm defect was reconstructed by 3 cables of sural grafts and an additional 1.5-cm bridge graft was placed between the presumed median and ulnar motor fascicles dissected according to the topographic anatomy as described by Williams and Jabaley in 198618 (Fig. 2). We tested the dissected motor fascicles of the median nerve with a nerve stimulator before suturing the graft to confirm that it was the motor branch. On follow-up 6 months after the surgery, there was returning sensation in the proximal part of the palm but no motor function was exhibited. Three months later, weak finger abduction and adduction (M3) were ob-
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ment of this patient 9 months after the surgery is demonstrated in the video (this video may be viewed at the Journal’s Web site, www.jhandsurg.org). EMG done at that time showed a greater response in this muscle after stimulation of the median nerve than after stimulation of the regenerating ulnar nerve.
FIGURE 2: A Motor branches of both the median and ulnar nerves dissected from the main nerve at the wrist and a double end-to-side nerve graft sutured to these branches. A red arrow marks the bridge graft. The motor branch of the donor nerve (here, the median nerve was tested by electrical stimulation before graft suture). B Magnification of the bridge graft sutured to the motor branches of the median and ulnar nerves after opening a perineural window.
served with minimal improvement of the intermetacarpal hollowness. Electromyelography done at this time confirmed starting regeneration of the abductor digiti minimi muscle from the repaired ulnar nerve but no conduction through the nerve graft. Case 3 A 49-year-old woman had a puncture injury by broken glass at the medial aspect of the distal part of the left arm with complete injury of the ulnar nerve. She was seen 2 months after the trauma and was then operated upon; the nerve could be secondarily repaired. A double end-to-side graft (2 cm) was inserted between the motor branches of the medial and ulnar nerves at the wrist through a perineural window as described in case 2 (Fig. 3A). At 4 months after the surgery, because Tinel’s sign of the ulnar nerve repair was still at the proximal part of the forearm, there was not yet return of sensation but some contraction could be elicited at the abductor digiti minimi (M1). The power of the hand muscle progressively increased with time to reach an M4 9 months after the repair (Fig. 3B, C). The postoperative move-
Case 4 An 8-year-old girl presented to the emergency room with a cut wound on the left cubital fossa after a fall while holding a glass bottle. The patient also had a ruptured left globe and multiple cuts in the left facial nerve. The cut median nerve was directly sutured and a sural nerve was harvested for grafting of the associated facial nerve injury, as well as a bridge graft between the motor fascicles of the median and ulnar nerves at the wrist through perineural windows. Ten weeks after the surgery, there was a positive Tinel’s sign across the wrist as well as in the proximal forearm across the repaired median nerve at the elbow. There was a weak abduction of the thumb (M2). Four months after the trauma, there was a stronger abduction of the thumb (M3) as well as flexion of the DIP joint of the index finger (Fig. 4). Electromyelogram and nerve conduction studies showed good response of the abductor pollicis brevis from both the regenerating median nerve across the repair at the elbow and the axons crossing the bridge graft from the ulnar nerve at the wrist (Fig. 5). The ulnarly innervated muscles of the hand and sensation in the ulnar side of the hand were not affected. There was also minimal muscle wasting compared with the other hand. DISCUSSION Collateral axonal sprouting is now accepted as a real phenomenon. Axonal regeneration can be seen at the proximal end of the grafted nerve as early as 48 hours after the creation of an epineural window.15 Although this sprouting can occur without removing the epineural sheath,2 the presence of Schwann-cell basement membrane, perineural-cell basement membrane, perineuralcell layer, and epineural connective tissue forms a barrier for axonal regeneration into the graft in experimental rats.4,10,19 In human limbs, the presence of thick connective tissue in and around major nerve trunk may further reduce the likelihood of axonal sprouting.10 A perineural window may thus be more effective than epineural window in allowing the nerves to the graft to sprout. In the cases presented here, because sensory recovery is usually expected after repair of high-median or ulnar nerve
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FIGURE 3: Case 3. A Bridge graft (black arrows) in anterior aspect of the wrist region sutured to the motor branch of the median and ulnar nerves (yellow arrows). Postoperative views showing abduction B and adduction of the fingers C 6 months after surgery.
FIGURE 4: Case 4. Postoperative photographs showing opposition of the thumb.
injuries, we performed only a motor-to-motor coaptation using a single cable graft. This was more effective than in the previous report by Kayikcioglu et al,10 in which 4 cables were used to bridge the whole median to the ulnar nerves above the wrist through epineural windows regardless of the motor and sensory distribution of the fascicles. This technique is effective for several reasons. First, neurorraphy is performed for the motor fascicles of the nerve, avoiding sensory “contamination” as much as possible and allowing regeneration to the motor fibers only. Second, a perineural window with removal of most of the connective tissue barrier present in the human peripheral nerves may allow more collateral sprouting into the graft. Third, a short graft
FIGURE 5: Case 4. EMG done 4 months after nerve repair showing good motor response with a latency of 3.9 ms detected in the abductor pollicis brevis muscle after stimulation of the median nerve, indicating good conduction across the bridge graft, as well as after stimulation of the ulnar nerve, indicating regenerating fibers across the repair.
near the motor end plates of the denervated muscle shortens the distance of nerve regeneration and thus reduces motor end plate and muscle atrophy by decreasing the duration of denervation. In the first case, the motor nerves were joined by the graft more distally in the hand; however, the motor nerve of the ulnar nerve lies deep in the palm and its dissection is difficult and time-consuming. The median and ulnar nerves at the wrist are superficial and their dissection is easier. Dissection of the motor nerves in the last 3 cases was done according to the internal topographic anatomy of the nerve as described by Williams and Jabaley18 and confirmed by intraoperative electrical stimulation of the
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donor nerve. Inaccuracy in dissecting the recipient motor fascicles separately may have been the cause of failure of 1 of our cases. Failure in this case may also be attributed to the delay in treatment, which was more than 6 months after the injury. The presence of Wallerian degeneration in the recipient nerve 6 months after the injury may reduce the amount of neurotropic factors that stimulate axonal sprouting from the normal nerve. However, this procedure should not be omitted even after a long denervation because it may improve muscle function without affecting the muscles that the donor nerve supplies. In the present series, there was no clinically detected dysesthesias or donor muscle weakness. This is also well documented by several experimental studies in which neither the muscle fibers nor the contractile force of the donor muscles were affected by the end-to-side suture of a nerve graft through a perineural window.4,14,20 –23 This finding is in contradiction with neurotization with deliberate axotomy of the donor nerve, in which muscle function was usually affected. This procedure was intended to prevent intrinsic muscle atrophy until the proximal nerve regeneration can reach these muscles. In 2 cases (cases 1 and 3, with a follow-up of 1 year and 9 months, respectively), however, EMG showed that the muscles were reinnervated only by regenerated fibers from the uninjured nerve. In only 1 patient the muscles were stimulated by both the median and ulnar nerve. Clinically and by EMG examination, it was not apparent which nerve was the predominant supply to these muscles. This technique is thus mainly indicated in high peripheral nerve injury or in secondary cases when recovery of the intrinsic muscle of the hand is not expected after end-to-end repair or graft. Although axonotmesis may produce more nerve sprouting in the bridge graft and better recovery in the denervated muscle, it runs the risk of dysfunction in the donor muscle and loss of hand function. However, experimental and clinical studies have shown that the epineural or perineural window does not seem to carry the same risk. In this series, the bridge graft did not seem to clinically affect the donor nerve muscle. It did not considerably increase the surgical time or affect the regenerating repaired nerve. REFERENCES 1. Aird RB, Naffziger HC. The pathology of human striated muscle following denervation. J Neurosurg 1953;10:216 –227. 2. Viterbo F, Trindade JC, Hoshino K, Neto AM. Latero-terminal neurorrhaphy without removal of the epineural sheath: an experimental study in rats. Rev Paul Med 1992;110:267–275.
3. Viterbo F, Trindade JC, Hoshino K, Neto AM. End-to side neurorrhaphy with removal of the epineural sheath. Plast Reconstr Surg 1994;94:1038 –1047. 4. Noah EM, Williams A, Jorghenson C, Skoulis TG, Terzis JK. End-to-side neurorrhaphy: a histologic amd morphometric study of axonal sprouting into an end-to-side nerve graft. J Reconstr Microsurg 1997;13:99 –106. 5. Kalliainen LK, Cederna PS, Kuzon WM. Mechanical function of muscle reinnervated by end-to-side neurorrhaphy. Plast Reconstr Surg 1999;103:1919 –1927. 6. May M, Sobol SM, Mester SJ. Hypoglossal-facial nerve interpositional-jump graft for facial reanimation without tongue atrophy. Otolaryngol Head Neck Surg 1991;104:818 – 825. 7. Endo T, Hata J, Nakayama Y. Variations on the “baby-sitter” procedure for reconstruction of facial paralysis. J Reconstr Microsurg 2000;16:37– 43. 8. Yong-Xiang L, Tipei W, Huang F. Preliminary investigation of treatment of ulnar nerve defect by end-to-side neurorrhaphy. Chinese J Reparative Reconstr Surg 1997;11:338 –339. 9. Kostakoglu N. Motor and sensory reinnervation in the hand after an end-to side median to ulnar nerve coaptation in the forearm. Br J Plast Surg 1999;52:404 – 407. 10. Kayikcioglu A, Karamursel S, Agoaglu G, Kecick A, Celiker R, Cetin A. End-to-side neurorrhaphy of the ulnar to median nerves at the wrist: report of two cases without sensory or motor improvement. Ann Plast Surg 2000;45:641– 643. 11. Mennen U. End-to-side nerve suture: in clinical practice. Hand Surg 2003;8A:33– 42. 12. Ogun TC, Ozdemir M, Senaran H, Ustun ME. End to side neurorrhaphy as a salvage procedure for irreparable nerve injuries: technical note. J Neurosurg 2003;99:180 –185. 13. Yuksel F, Peker F, Velikoz B. Two applications of end-to-side neurorrhaphy in severe upper extremity nerve injuries. Microsurgery 2004;24:363–368. 14. Mouilhade F, Barbary S, Apard T, Dautel G. End-to-side neurorrhaphy for median nerve repair after elbow tumor resection: case report. J Hand Surg 2009;34A:83– 86. 15. Viterbo F, Trindade JC, Hoshino K, Mazzoni A. Two end-to-side neurorrhaphy and nerve grafts with removal of epineural sheath: experimental study in rats. Br J Plast Surg 1994;47:75– 80. 16. Viterbo F. A new method for treatment of facial palsy: the cross-face nerve transplantation with end-to-side neurorrhaphy. Rev Soc Bras Cir Plast Est Reconstr 1993;8:29 –35. 17. Koh KS, Kim J, Kim CJ, Kwun BD, Kim S. Hypoglossal-facial crossover in facial nerve palsy: pure end-to-side anastomosis technique. Br J Plast Surg 2002;55:25–31. 18. Williams HB, Jabaley ME. The importance of internal anatomy of the peripheral nerves to nerve repair in the forearm and hand. Hand Clin 1986;2:689 –707. 19. Okajima S, Terzis JK. Ultra structure of early axonal regeneration in an end-to-side neurorrhaphy model. J Reconstr Microsurg 2000;16: 313–326. 20. Lundborg G, Zhao Q, Kanje M, Danielsen N, Kerns JM. Can sensory and motor sprouting be induced from intact peripheral nerve by end-to-side anastomosis? J Hand Surg 1994;19B:227–282. 21. Giovanoli P, Koller R, Meuli-Simmen C, Rab M, Haslik W, Mittlböck M, et al. Functional and morphometric evaluation of end-toside neurorrhaphy for muscle reinnervation. Plastic Reconstr Surg 2000;106:383–392. 22. Cederna PS, Kalliainen LK, Urbanchek MG, Rovak JM, Kuzon WM. Donor muscle structure and function after end-to-side neurorrhaphy. Plast Reconstr Surg 2001;107:789 –796. 23. Zhang Z, Johnson EO, Vekris MD, Zoubos AB, Bo J, Beris AE, et al. Repair of the main trunk of the upper limb with end-to-side neurorrhaphy an experimental study in rabbits. Microsurgery 2006; 26:245–252.
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Intrinsic Hand Muscle Reinnervation by Median-Ulnar End-to-Side Bridge Nerve Graft: Case Report M. Magdi Sherif, MD, Adel H. Amr, MD Recovery of either the motor or sensory functions has not been consistently achieved in upper extremity end-to-side neurorrhaphy; this technique was only indicated when more conventional nerve repair was not possible. In most studies, the whole median or ulnar nerve was used for end-to-side neurotization. In this report, we present 4 cases of high-median or ulnar nerve laceration in which a nerve graft was placed end-to-side between the median and ulnar motor fascicles close to the wrist. At 4 months after surgery, 3 of 4 patients began to recover active movement of the affected small muscles of the hand. EMG and nerve conduction studies confirmed that nerve conduction was through the nerve grafts. (J Hand Surg 2010;35A:446–450. Copyright © 2010 by the American Society for Surgery of the Hand. All rights reserved.) Key words High-median/ulnar nerve injury, double end-to-side nerve graft, bridge graft, hand intrinsic muscles reinnervation.
urrently, the most accepted treatment of peripheral nerve injury is a primary, tension-free repair whenever possible. In high or old median or ulnar nerve lesions, sensory improvement is expected after nerve repair, but intrinsic muscle recovery is rarely satisfactory. Muscle atrophy and fibrosis progress in proportion to the duration of denervation.1 Because the regenerating axons grow at a slow rate, they reach their target end organ after the muscle has atrophied and has become unresponsive to stimuli. A variety of methods have been used to enhance the rate or increase the number of regenerating axons. These include pharmacological agents, external electrical stimulation, implanted electrodes, and transplantation of embryonic motor neurons or sensory ganglion
C
From the Department of Plastic Surgery, Ain Shams University, Cairo, Egypt. The authors are grateful to the anonymous reviewers whose comments significantly helped improve the presentation. Received for publication May 22, 2009; accepted in revised form October 28, 2009. No benefits in any form have been received or will be received related directly or indirectly to the subject of this article. Corresponding author: M. Magdi Sherif, MD, Department of Plastic Surgery, Ain Shams University, 2-A Alsayed abou Shady Street, Heliopolis, Cairo 11361, Egypt; e-mail: magdisherif@ yahoo.com. 0363-5023/10/35A03-0014$36.00/0 doi:10.1016/j.jhsa.2009.10.033
446 䉬 © ASSH 䉬 Published by Elsevier, Inc. All rights reserved.
into the cut nerve. During the past decade, numerous studies have demonstrated the effectiveness of end-toside neurorrhaphy for muscle reinnervation in animal models.2–5 In clinical studies, this technique has been applied successfully to produce temporary innervation of the facial muscles and prevent denervation atrophy until the axons of a cross facial nerve graft reach the paralyzed side of the face.6,7 However, the results of end-to-side median-ulnar neurorrhaphy have not always been successful, with more recovery of the large proximal muscles8 –11 than in the intrinsic hand muscles.10,11 Sensory recovery in the hand after this procedure is also unpredictable; it varies from protective sensation9,12–14 to full recovery,8 even with normal anatomical orientation.11 Therefore, this technique has been recommended only when more conventional repair is not possible.10 In most of the previous studies, the whole injured median or ulnar nerve was used for end-to-side suture to the uninjured nerve.8,9 –11 In one report,10 nerve grafts were used to connect the 2 nerves without respect to the sensory and motor arrangement of the fascicles. Experimentally, it has been shown that axons can also grow through a nerve graft joining 2 adjacent nerves by 2 end-to-side neurorrhaphies with or without deliberate axonotomy of the donor nerve.2–15 This was used clin-
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ically in facial palsy to produce temporary innervation of the facial muscles without affecting the muscles of the donor nerve.6,16,17 To shorten the distance axons have to travel to reach the intrinsic muscles and to prevent their denervation atrophy, we used an end-to-side nerve graft between the intrinsic motor fascicles of the median and ulnar nerves near the wrist in 4 cases of high-median and ulnar nerve laceration. CASE REPORTS Case 1 A 34-year-old man sustained a road traffic accident with deep abrasion of the left forearm, exposing the median nerve at the elbow, which was completely cut. The area was debrided followed by flap coverage of the exposed nerve. After the area completely healed, the infection subsided and the scars softened, and the patient was operated on again. The median nerve was grafted using 4 sural nerve cables, each measuring 6 cm for the innervation of the long flexors and to regain hand sensation. To avoid atrophy of the thenar muscles, we used another graft to bridge the motor branches of the median and ulnar nerves in the palm through 2 additional small incisions located over the expected motor branches of both nerves. In this area, the motor nerve is completely separate from the sensory branches and the regenerating axons will run through the shortest possible distance. An epineural window was performed in each nerve and a single cable 3 cm long was sutured end-to-side with 10-0 suture. At 1.5 months after the surgery, Tinel’s sign of regenerating axons through the bridge graft was noted near the thenar eminence. One month later, there was some recovery in the thenar bulk with weak active abduction and opposition of the thumb. At the 4th postoperative month, the power of these muscles could be graded as M3 to M4 (Fig. 1). EMG and nerve conduction studies done at that time showed some recovery of the flexor carpi radialis after stimulation of the left median nerve at the elbow (no activity at rest and complete interference pattern with average motor units in volition), indicating reinnervation of the flexor muscles. Stimulation of the ulnar nerve at the wrist gave a powerful muscle-evoked response for the abductor pollicis brevis. In contrast, stimulation of the median nerve at the wrist and elbow gave no response at this muscle, indicating its reinnervation through the bridge graft from the motor branch of the ulnar nerve. One year after the surgery, while Tinel’s sign of the regenerating median nerve was still at the wrist level, the patient was able to use his computer normally.
FIGURE 1: Case 1 at 1 year after bridge graft, showing functioning abductor pollicis brevis against resistance.
EMG done at that time showed no response of the abductor pollicis brevis on stimulation of the median nerve; there was also good response on stimulation of the ulnar nerve. Case 2 A 23-year-old man was injured by broken glass at the middle part of the left forearm. The wound was sutured primarily, but the patient noticed weakness of the hand with loss of sensation of the ulnar 1-1/2 fingers. The patient was seen for the first time 6 months after the injury. Examination at that time revealed a complete ulnar nerve injury with wasting of the interosseous muscles and partial clawing of the hand. At surgery, a 5-cm defect was reconstructed by 3 cables of sural grafts and an additional 1.5-cm bridge graft was placed between the presumed median and ulnar motor fascicles dissected according to the topographic anatomy as described by Williams and Jabaley in 198618 (Fig. 2). We tested the dissected motor fascicles of the median nerve with a nerve stimulator before suturing the graft to confirm that it was the motor branch. On follow-up 6 months after the surgery, there was returning sensation in the proximal part of the palm but no motor function was exhibited. Three months later, weak finger abduction and adduction (M3) were ob-
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ment of this patient 9 months after the surgery is demonstrated in the video (this video may be viewed at the Journal’s Web site, www.jhandsurg.org). EMG done at that time showed a greater response in this muscle after stimulation of the median nerve than after stimulation of the regenerating ulnar nerve.
FIGURE 2: A Motor branches of both the median and ulnar nerves dissected from the main nerve at the wrist and a double end-to-side nerve graft sutured to these branches. A red arrow marks the bridge graft. The motor branch of the donor nerve (here, the median nerve was tested by electrical stimulation before graft suture). B Magnification of the bridge graft sutured to the motor branches of the median and ulnar nerves after opening a perineural window.
served with minimal improvement of the intermetacarpal hollowness. Electromyelography done at this time confirmed starting regeneration of the abductor digiti minimi muscle from the repaired ulnar nerve but no conduction through the nerve graft. Case 3 A 49-year-old woman had a puncture injury by broken glass at the medial aspect of the distal part of the left arm with complete injury of the ulnar nerve. She was seen 2 months after the trauma and was then operated upon; the nerve could be secondarily repaired. A double end-to-side graft (2 cm) was inserted between the motor branches of the medial and ulnar nerves at the wrist through a perineural window as described in case 2 (Fig. 3A). At 4 months after the surgery, because Tinel’s sign of the ulnar nerve repair was still at the proximal part of the forearm, there was not yet return of sensation but some contraction could be elicited at the abductor digiti minimi (M1). The power of the hand muscle progressively increased with time to reach an M4 9 months after the repair (Fig. 3B, C). The postoperative move-
Case 4 An 8-year-old girl presented to the emergency room with a cut wound on the left cubital fossa after a fall while holding a glass bottle. The patient also had a ruptured left globe and multiple cuts in the left facial nerve. The cut median nerve was directly sutured and a sural nerve was harvested for grafting of the associated facial nerve injury, as well as a bridge graft between the motor fascicles of the median and ulnar nerves at the wrist through perineural windows. Ten weeks after the surgery, there was a positive Tinel’s sign across the wrist as well as in the proximal forearm across the repaired median nerve at the elbow. There was a weak abduction of the thumb (M2). Four months after the trauma, there was a stronger abduction of the thumb (M3) as well as flexion of the DIP joint of the index finger (Fig. 4). Electromyelogram and nerve conduction studies showed good response of the abductor pollicis brevis from both the regenerating median nerve across the repair at the elbow and the axons crossing the bridge graft from the ulnar nerve at the wrist (Fig. 5). The ulnarly innervated muscles of the hand and sensation in the ulnar side of the hand were not affected. There was also minimal muscle wasting compared with the other hand. DISCUSSION Collateral axonal sprouting is now accepted as a real phenomenon. Axonal regeneration can be seen at the proximal end of the grafted nerve as early as 48 hours after the creation of an epineural window.15 Although this sprouting can occur without removing the epineural sheath,2 the presence of Schwann-cell basement membrane, perineural-cell basement membrane, perineuralcell layer, and epineural connective tissue forms a barrier for axonal regeneration into the graft in experimental rats.4,10,19 In human limbs, the presence of thick connective tissue in and around major nerve trunk may further reduce the likelihood of axonal sprouting.10 A perineural window may thus be more effective than epineural window in allowing the nerves to the graft to sprout. In the cases presented here, because sensory recovery is usually expected after repair of high-median or ulnar nerve
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FIGURE 3: Case 3. A Bridge graft (black arrows) in anterior aspect of the wrist region sutured to the motor branch of the median and ulnar nerves (yellow arrows). Postoperative views showing abduction B and adduction of the fingers C 6 months after surgery.
FIGURE 4: Case 4. Postoperative photographs showing opposition of the thumb.
injuries, we performed only a motor-to-motor coaptation using a single cable graft. This was more effective than in the previous report by Kayikcioglu et al,10 in which 4 cables were used to bridge the whole median to the ulnar nerves above the wrist through epineural windows regardless of the motor and sensory distribution of the fascicles. This technique is effective for several reasons. First, neurorraphy is performed for the motor fascicles of the nerve, avoiding sensory “contamination” as much as possible and allowing regeneration to the motor fibers only. Second, a perineural window with removal of most of the connective tissue barrier present in the human peripheral nerves may allow more collateral sprouting into the graft. Third, a short graft
FIGURE 5: Case 4. EMG done 4 months after nerve repair showing good motor response with a latency of 3.9 ms detected in the abductor pollicis brevis muscle after stimulation of the median nerve, indicating good conduction across the bridge graft, as well as after stimulation of the ulnar nerve, indicating regenerating fibers across the repair.
near the motor end plates of the denervated muscle shortens the distance of nerve regeneration and thus reduces motor end plate and muscle atrophy by decreasing the duration of denervation. In the first case, the motor nerves were joined by the graft more distally in the hand; however, the motor nerve of the ulnar nerve lies deep in the palm and its dissection is difficult and time-consuming. The median and ulnar nerves at the wrist are superficial and their dissection is easier. Dissection of the motor nerves in the last 3 cases was done according to the internal topographic anatomy of the nerve as described by Williams and Jabaley18 and confirmed by intraoperative electrical stimulation of the
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donor nerve. Inaccuracy in dissecting the recipient motor fascicles separately may have been the cause of failure of 1 of our cases. Failure in this case may also be attributed to the delay in treatment, which was more than 6 months after the injury. The presence of Wallerian degeneration in the recipient nerve 6 months after the injury may reduce the amount of neurotropic factors that stimulate axonal sprouting from the normal nerve. However, this procedure should not be omitted even after a long denervation because it may improve muscle function without affecting the muscles that the donor nerve supplies. In the present series, there was no clinically detected dysesthesias or donor muscle weakness. This is also well documented by several experimental studies in which neither the muscle fibers nor the contractile force of the donor muscles were affected by the end-to-side suture of a nerve graft through a perineural window.4,14,20 –23 This finding is in contradiction with neurotization with deliberate axotomy of the donor nerve, in which muscle function was usually affected. This procedure was intended to prevent intrinsic muscle atrophy until the proximal nerve regeneration can reach these muscles. In 2 cases (cases 1 and 3, with a follow-up of 1 year and 9 months, respectively), however, EMG showed that the muscles were reinnervated only by regenerated fibers from the uninjured nerve. In only 1 patient the muscles were stimulated by both the median and ulnar nerve. Clinically and by EMG examination, it was not apparent which nerve was the predominant supply to these muscles. This technique is thus mainly indicated in high peripheral nerve injury or in secondary cases when recovery of the intrinsic muscle of the hand is not expected after end-to-end repair or graft. Although axonotmesis may produce more nerve sprouting in the bridge graft and better recovery in the denervated muscle, it runs the risk of dysfunction in the donor muscle and loss of hand function. However, experimental and clinical studies have shown that the epineural or perineural window does not seem to carry the same risk. In this series, the bridge graft did not seem to clinically affect the donor nerve muscle. It did not considerably increase the surgical time or affect the regenerating repaired nerve. REFERENCES 1. Aird RB, Naffziger HC. The pathology of human striated muscle following denervation. J Neurosurg 1953;10:216 –227. 2. Viterbo F, Trindade JC, Hoshino K, Neto AM. Latero-terminal neurorrhaphy without removal of the epineural sheath: an experimental study in rats. Rev Paul Med 1992;110:267–275.
3. Viterbo F, Trindade JC, Hoshino K, Neto AM. End-to side neurorrhaphy with removal of the epineural sheath. Plast Reconstr Surg 1994;94:1038 –1047. 4. Noah EM, Williams A, Jorghenson C, Skoulis TG, Terzis JK. End-to-side neurorrhaphy: a histologic amd morphometric study of axonal sprouting into an end-to-side nerve graft. J Reconstr Microsurg 1997;13:99 –106. 5. Kalliainen LK, Cederna PS, Kuzon WM. Mechanical function of muscle reinnervated by end-to-side neurorrhaphy. Plast Reconstr Surg 1999;103:1919 –1927. 6. May M, Sobol SM, Mester SJ. Hypoglossal-facial nerve interpositional-jump graft for facial reanimation without tongue atrophy. Otolaryngol Head Neck Surg 1991;104:818 – 825. 7. Endo T, Hata J, Nakayama Y. Variations on the “baby-sitter” procedure for reconstruction of facial paralysis. J Reconstr Microsurg 2000;16:37– 43. 8. Yong-Xiang L, Tipei W, Huang F. Preliminary investigation of treatment of ulnar nerve defect by end-to-side neurorrhaphy. Chinese J Reparative Reconstr Surg 1997;11:338 –339. 9. Kostakoglu N. Motor and sensory reinnervation in the hand after an end-to side median to ulnar nerve coaptation in the forearm. Br J Plast Surg 1999;52:404 – 407. 10. Kayikcioglu A, Karamursel S, Agoaglu G, Kecick A, Celiker R, Cetin A. End-to-side neurorrhaphy of the ulnar to median nerves at the wrist: report of two cases without sensory or motor improvement. Ann Plast Surg 2000;45:641– 643. 11. Mennen U. End-to-side nerve suture: in clinical practice. Hand Surg 2003;8A:33– 42. 12. Ogun TC, Ozdemir M, Senaran H, Ustun ME. End to side neurorrhaphy as a salvage procedure for irreparable nerve injuries: technical note. J Neurosurg 2003;99:180 –185. 13. Yuksel F, Peker F, Velikoz B. Two applications of end-to-side neurorrhaphy in severe upper extremity nerve injuries. Microsurgery 2004;24:363–368. 14. Mouilhade F, Barbary S, Apard T, Dautel G. End-to-side neurorrhaphy for median nerve repair after elbow tumor resection: case report. J Hand Surg 2009;34A:83– 86. 15. Viterbo F, Trindade JC, Hoshino K, Mazzoni A. Two end-to-side neurorrhaphy and nerve grafts with removal of epineural sheath: experimental study in rats. Br J Plast Surg 1994;47:75– 80. 16. Viterbo F. A new method for treatment of facial palsy: the cross-face nerve transplantation with end-to-side neurorrhaphy. Rev Soc Bras Cir Plast Est Reconstr 1993;8:29 –35. 17. Koh KS, Kim J, Kim CJ, Kwun BD, Kim S. Hypoglossal-facial crossover in facial nerve palsy: pure end-to-side anastomosis technique. Br J Plast Surg 2002;55:25–31. 18. Williams HB, Jabaley ME. The importance of internal anatomy of the peripheral nerves to nerve repair in the forearm and hand. Hand Clin 1986;2:689 –707. 19. Okajima S, Terzis JK. Ultra structure of early axonal regeneration in an end-to-side neurorrhaphy model. J Reconstr Microsurg 2000;16: 313–326. 20. Lundborg G, Zhao Q, Kanje M, Danielsen N, Kerns JM. Can sensory and motor sprouting be induced from intact peripheral nerve by end-to-side anastomosis? J Hand Surg 1994;19B:227–282. 21. Giovanoli P, Koller R, Meuli-Simmen C, Rab M, Haslik W, Mittlböck M, et al. Functional and morphometric evaluation of end-toside neurorrhaphy for muscle reinnervation. Plastic Reconstr Surg 2000;106:383–392. 22. Cederna PS, Kalliainen LK, Urbanchek MG, Rovak JM, Kuzon WM. Donor muscle structure and function after end-to-side neurorrhaphy. Plast Reconstr Surg 2001;107:789 –796. 23. Zhang Z, Johnson EO, Vekris MD, Zoubos AB, Bo J, Beris AE, et al. Repair of the main trunk of the upper limb with end-to-side neurorrhaphy an experimental study in rabbits. Microsurgery 2006; 26:245–252.
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