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Distal Sensory Nerve Transfers in Lower-Type Injuries of the Brachial Plexus
SCIENTIFIC ARTICLE
Distal Sensory Nerve Transfers in Lower-Type Injuries of the Brachial Plexus Jayme A. Bertelli, MD, PhD
Purpose To report the results of sensory nerve transfers to reconstruct sensation on the ulnar side of the hand in lower-type palsies of the brachial plexus. Methods From 2007 to 2009, we operated on 6 men and 2 women with a lower-type injury of the brachial plexus and observed them for a minimum of 24 months. The mean interval between the injury and surgery was 8 months (SD ⫾ 8.6 mo). Before surgery, we documented anesthesia on the ulnar side of the hand in all patients. Donor nerves included cutaneous branches of the median nerve to the palm (n ⫽ 5) or the palmar cutaneous branch of the median nerve (n ⫽ 3). The ulnar proper digital nerve of the little finger was the recipient nerve. We evaluated sensory recovery by assessing static 2-point discrimination and sensation to Semmes-Weinstein monofilaments. Results According to the British Medical Council system of evaluation, 5 patients scored S3 and 3 scored S3⫹. Conclusions In lower-type injuries of the brachial plexus, transfer of median nerve branches that innervate the palm of the hand to the ulnar proper digital nerve of the little finger predictably restored protective sensation on the ulnar side of the hand. (J Hand Surg 2012;37A:1194–1199. Copyright © 2012 by the American Society for Surgery of the Hand. All rights reserved.) Type of study/level of evidence Therapeutic IV. Key words Brachial plexus, lower root palsy of the brachial plexus, nerve transfer, sensory reconstruction. brachial plexus injuries can be roughly classified into upper- and lower-type injuries. With uppertype injuries, the C5 and possibly C6 and C7 roots are affected, and despite clinical motor paralysis, hand sensation is largely preserved and no sensory reconstruction is needed.1 Conversely, with lower-type injuries, the T1 and, possibly, C8 and C7 roots are involved. The ulnar border of the hand is insensate and would likely
A
CCORDING
TO
ROOT
INVOLVEMENT,
From the Center of Biological and Health Sciences, Department of Neurosurgery, University of the South of Santa Catarina (Unisul), Tubarão; and the Department of Orthopedic Surgery, Governador Celso Ramos Hospital, Florianópolis, Santa Catarina, Brazil. Received for publication November 29, 2011; accepted in revised form February 27, 2012. No benefits in any form have been received or will be received related directly or indirectly to the subject of this article. Corresponding author: Jayme A. Bertelli, MD, PhD, Rua Newton Ramos 70, Apto 901, Florianópolis-SC, 88015395, Brazil; e-mail: [email protected]. 0363-5023/12/37A06-0014$36.00/0 http://dx.doi.org/10.1016/j.jhsa.2012.02.047
1194 䉬 © ASSH 䉬 Published by Elsevier, Inc. All rights reserved.
benefit from sensory reconstruction.1 Loss of sensation on the ulnar side of the hand predisposes to injury, because the ulnar side usually is used to support the hand while the radial fingers carry out manipulation. Sensation on the ulnar border of the hand is particularly important if the hand is ever placed on a potentially damaging surface, such as a hot stove. Also, because of the absence of sensation on the tip of the little finger, minor repetitive trauma may be neglected, resulting in skin breakdown and infections. In lower-type palsies, the roots are always avulsed, and reconstructive surgery for hand motion relies on nerve and tendon transfers.2– 4 Nerve transfers for motor reconstruction of median and ulnar nerve lesions have been reported.5–7 However, specifically for sensory reconstruction in lower-type lesions of the brachial plexus, we identified 3 reports. Oberlin et al8 and Goubier and Teboul9 transferred the lateral antebrachial cutaneous nerve with the help of a long graft to the
DISTAL SENSORY NERVE TRANSFERS
dorsal branch of the ulnar nerve. Doi et al10 transferred intercostal nerves to the ulnar nerve. We report the results of direct nerve transfers for sensory reconstruction along the ulnar border of the hand in lower-type injuries of the brachial plexus. Donor nerves included cutaneous branches of the median nerve to the palm or the palmar cutaneous branch of the median nerve. The ulnar proper digital nerve of the little finger was the recipient nerve. MATERIALS AND METHODS In advance of any data collection, the local ethics committee approved the protocol of the study. Patients provided written informed consent before participation, in accordance with the Declaration of Helsinki guiding biomedical research involving human subjects. From 2007 to 2009, we operated on 6 men and 2 women with lower-type injuries of the brachial plexus and observed them for a minimum of 24 months (Table 1). Their average age was 34 years (SD ⫾15 y), and the mean interval between the initial injury and surgery was 8 months (SD ⫾ 8.6 mo). All had lower root avulsion documented by computed tomographic myelography (n ⫽ 4) or magnetic resonance imaging (n ⫽ 4). All presented with a Horner sign, except for 1 patient with a prosthetic eye replacement resulting from a previous injury. In each patient, we demonstrated anesthesia on the ulnar side of the hand by the absence of perception of a 33.1-g/mm2 monofilament, and of pain when the skin was pinched with flat forceps. We reconstructed sensation along the ulnar border of the hand using distal nerve transfers. If perception of 19.3-g/mm2 Semmes-Weinstein monofilaments (protective sensation) was preserved in the center of the palm, we used as donors cutaneous branches of the median nerve to the skin (Fig. 1) just distal to the carpal tunnel. We used these median nerve cutaneous branches either isolated (n ⫽ 3) or combined (n ⫽ 2) with fascicles of the ulnar proper digital nerve of the index finger (Fig. 2) if the caliber of the cutaneous branches failed to cover the entire surface of the distal stump of the ulnar proper digital nerve of the little finger. Before harvesting fascicles of the proper digital nerve of the index finger, we determined that pulp sensation was normal on monofilament testing (ie, preserved perception of a 1.5-g/mm2 monofilament). In the case of absent protective sensation over the zone just distal to the carpal tunnel, we used the palmar cutaneous branch of the median nerve for transfer, provided that perception of a 19.3-g/mm2 monofilament was preserved over the thenar region (n ⫽ 3). After proximal dissection, the ulnar proper digital nerve
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of the little finger was the recipient nerve in these 3 patients (Fig. 3). At final evaluation, we tested for static 2-point discrimination on the tip of the small finger using a DiskCriminator testing device (Connecticut Bioinstruments, Baltimore, MD). On the ulnar border of the little finger and hand, we investigated sensory thresholds using Semmes-Weinstein monofilaments in accordance with methods reported elsewhere.7 We used 4 sets of monofilaments. According to the manufacturer (Sorri, Bauru, Sao Paulo, Brazil), the 0.05, 0.2, 2.0, and 4.0 monofilaments produce pressures of 1.5, 11.1, 19.3, and 33.1 g/mm2, respectively. To map the reinnervated cutaneous territory, we considered referred sensation corresponding to the donor nerve primary zone of innervation as a guideline. We grasped the skin on the ulnar side of the hand with a flat forceps with increasing firmness until pain was perceived either in the central part of the palm or in the thenar region. This denoted that reinnervation stemmed from our nerve transfer rather than from spontaneous regeneration of adjacent nerves. We repeated this all over the ulnar border of the hand. Then, with a skin marker, we delineated the cutaneous territory presenting referred sensation, for photographing. We also determined results according to British Medical Research Council standards.11 We rated the patient’s score S3 when that patient perceived contact from a 33.1-g/mm2 monofilament, and S3⫹ when he perceived 2 points less than 10 mm apart. For detection of donor site deficits after nerve harvesting, we applied monofilament testing on the tip of the index finger, the thenar region, and the central part of the palm. For the thenar region and palm, we only applied 19.3-g/mm2 monofilaments. An examiner blinded to which nerve had been transferred conducted final sensory assessments. RESULTS All patients improved from baseline (Table 1), including those with longstanding lesions. The territory of sensory recovery extended to the tip of the little finger and the ulnar border of the hand. We observed recovery of 2-point discrimination in 3 of the 8 patients. In 2 of these 3 patients, we had connected branches of the median nerve to the palm together with fascicles of the ulnar proper digital nerve of the index to the ulnar proper digital nerve of the little finger. In the remaining case, we only used branches of the median nerve to the palm. Preoperatively or shortly after surgery, 4 of the 8 patients experienced a burn in the hypothenar region (n ⫽ 1) or on the little finger (n ⫽ 3).
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TABLE 1.
Patient Data Summary
Age/Sex
1
20, M
3
Palmar branch of median nerve to ulnar proper digital nerve of little finger
24
2
18, M
28
Cutaneous branches to palm plus fascicles of ulnar proper digital nerve of index to ulnar proper digital nerve of little finger
48
3
48, M
12
Cutaneous branches to palm to ulnar proper digital nerve of little finger
24
4
20, M
4
Cutaneous branches to palm plus fascicles of ulnar proper digital nerve of index to ulnar proper digital nerve of little finger
24
5
30, M
4
Palmar branch of median nerve to ulnar proper digital nerve of little finger
36
6
55, F
4
Palmar branch of median nerve to ulnar proper digital nerve of little finger
36
7
28, F
6
Cutaneous branches of palm to ulnar proper digital nerve of little finger
24
8
50, M
3
Cutaneous branches to palm to ulnar proper digital nerve of little finger
27
Surgery
BMRC, British Medical Research Council; ⫹, pain perception recovery.
Evaluation After Surgery (mo)
2-Point Discrimination (mm)
7
8
7
Monofilaments (Manufacturer’s Calculated Pressure [g/mm2])
Pain Perception
Territory of Reinnervation
BMRC
⫹
Distal ulnar border of hand plus little finger
S3
19.3
⫹
Distal ulnar border of hand plus little finger
S3⫹
11.1
⫹
Distal ulnar border of hand plus little finger
S3
19.3
⫹
Distal ulnar border of hand plus little finger
S3⫹
⫹
Distal ulnar border of hand plus little finger
S3
33.1
⫹
Distal ulnar border of hand plus little finger
S3
19.3
⫹
Distal ulnar border of hand plus little finger
S3⫹
19.3
⫹
Distal ulnar border of hand plus little finger
S3
DISTAL SENSORY NERVE TRANSFERS
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Patient
Interval Between Accident and Surgery (mo)
DISTAL SENSORY NERVE TRANSFERS
FIGURE 1: Intraoperative photograph of the palmar region of a left hand demonstrating transfer of a cutaneous branch of the median nerve (CB) to the ulnar proper digital nerve of the little finger (PL). P, ulnar proper digital nerve of the index finger. In the inset, we show the nerves after microsurgical coaptation.
FIGURE 2: Intraoperative view of the palmar region of a left hand, showing transfer (black arrow) of a cutaneous branch to the palm together with 2 fascicles of the ulnar proper digital nerve to the index to the ulnar proper digital nerve of the little finger. In the inset, we show the skin incisions used for the surgical procedure. P, ulnar proper digital nerve of the index finger.
Afterward, no other injuries on the ulnar side of the hand occurred. During our assessment for nociceptive recovery, we demonstrated referred sensation in all patients. However, none reported referred sensation adversely affecting daily activities. There were no donor site deficits on the index finger or loss of protective sensation in the palm or thenar region. Pain reports were absent.
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FIGURE 3: Intraoperative view of the left wrist showing transfer of the palmar cutaneous branch of the median nerve (PM) to the ulnar proper digital nerve of the little finger (PL). We used the incision at the distal palmar crease to correct metacarpophalangeal hyperextension. We also located the ulnar proper digital nerve of the little finger through this incision. We elongated the wrist incision to transfer the brachialis via a tendon graft to the flexor pollicis longus and flexor digitorum profundus tendons.
DISCUSSION In our series of 8 patients, transfer of either the palmar branch or cutaneous branches to the palm of the median nerve restored at least S3 sensation on the ulnar side of the hand. We based our indications to use one or the other nerve on preoperative screening for preserved sensation on the palm. Our first choice as donor nerves was the cutaneous branches of the median nerve in the palm because nerve coaptation is closer to cutaneous targets on the ulnar side of the little finger compared with nerve coaptation at the wrist, in which case the palmar cutaneous branch of the median nerve was the donor nerve. Lesions affecting the 3 lower roots of the brachial plexus tended to exhibit more extended sensory loss.1 However, even in such extended lesions, sensation over the thenar region was preserved, allowing for the use of the palmar cutaneous branch of the median nerve as the donor. In 3 patients, transfer of cutaneous branches of the median nerve, either combined with or separate from fascicles of the ulnar proper digital nerve to the index finger, restored 2-point discrimination on the tip of the little finger. The territory of cutaneous reinnervation included the ulnar border of the little finger and distal palm. After harvesting median nerve branches to the palm for transfer, we observed no donor site deficits or pain reports. Possibly, superimposed innervation exists between the palmar cutaneous branch of the median nerve
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DISTAL SENSORY NERVE TRANSFERS
and the lateral antebrachial cutaneous nerve, and between the palmar cutaneous branch of the median nerve and branches to the palm. When we harvested fascicles of the proper digital nerves to the index finger, normal sensation at the fingertip persisted. This is in agreement with our previous report in which we used fascicles of the proper digital nerves to the index finger to reinnervate skin flaps.12 According to the British Medical Research Council scale, S3 is related to return of superficial cutaneous pain and tactile sensibility.11 Because no objective parameter has been defined to represent superficial cutaneous pain and tactile sensibility, we used as a guideline the perception of 19.3-g/mm2 monofilament, which is related to protective sensation in the hand.13 Hence, in our analysis, a result scoring S3 meant that the patient recovered protective sensation at least. However, we believe that perception of 19.3 g/mm2 is not just the perception of a harmful stimulus. In fact, perception of 19.3 g/mm2 correlates positively with texture discrimination.14 In the diabetic foot, ulcers are associated with lack of perception of 10-g/mm2 monofilaments.15 However, testing sensation with heavier monofilaments may produce finger motion or reverberation of the stimuli on proximal zones. More than a century ago, Letiévant16 demonstrated that patients could perceive touching on totally necrotic skin on the fingertip due to mechanical stimulus perception in healthy proximal zones. Here, we believe that testing painful sensation with forceps would be preferable—in particular, if the amount of pressure on the forceps tip could be measured using a gauge. The next higher British Medical Research Council grade is S3⫹, which denotes some recovery of 2-point discrimination.11 However, 2-point discrimination may not effectively correlate to sensibility recovery.17 Jerosch-Herold18 observed that as much as 71% of 41 patients with repair of the median nerve at the wrist recovered no measurable 2-point discrimination 18 months after repair. This author considered that the 2-point discrimination test was not reliable to document recovery, which was more accurately documented by monofilaments screening. To determine the territory of cutaneous reinnervation, we tested nociceptive perception using forceps and referred sensation to the autonomous zone of the donor nerve. Faulty location is a common finding after sensory nerve transfer, in particular when different or distant zones are involved, as in our cases in which we crossed median and ulnar nerve branches.7 This does not mean that faulty location eliminates the benefits of nerve crossing. Patients can learn to cope with faulty location. In the set of sensory nerve crossing, Sperry19
believed that voluntary control, which depends on higher brain centers, can be learned: for instance, the removal of a painful stimulus applied to a reinnervated zone. This would result from learning experiences of fruitful or fruitless reactions. On the other hand, Sperry19 considered spinal reflexes not to be modifiable. In a series of 13 patients with lower-type injuries of the brachial plexus, Gobier and Teboul9 observed S2 recovery after transfer of the lateral antebrachial cutaneous nerve to the dorsal branch of the ulnar nerve with an intercalated 15-cm-long sural nerve graft. In 3 children aged 5.0, 6.5, and 7.0 years, with global obstetric brachial plexus injury, Ruchelsman et al20 divided the lateral antebrachial cutaneous nerve and implanted the proximal stump termino-laterally into the ulnar nerve. All 3 children recovered innervation on the ulnar border of the hand, as demonstrated by skin wrinkling after immersing the hands in warm water. Doi et al10 reported their results with intercostal nerve transfer to the ulnar nerve in 3 patients with lower-type brachial plexus injuries. Two of the patients recovered superficial pain and touch sensation, whereas the third patient did not. In 2 patients with brachial plexus injury who had partially recovered sensation in the middle finger (S3⫹), Brunelli21 transferred a proper digital nerve of the middle finger to the ulnar proper digital nerve of the little finger. In 1 of his patients, the end result was S2⫹; in the other it was S1. With our technique, we employed no nerve grafts and we performed nerve coaptation close to end organs. Likely, these 2 advantages contributed to our improved sensory recovery even many months after injury. Because of anesthesia along the ulnar border of the hand, the cases presented here theoretically could have been treated as high ulnar nerve lesions, but in our patients, the roots to the median nerve were also injured. Because we were concerned about donor site deficits, we elected not to harvest donor nerves of important zones, such as the entire ulnar proper digital nerve of the index finger, as proposed by Ozkan et al5 for pure ulnar nerve lesions. In a 13-year-old patient with ulnar and median nerve lesions in the arm, Turnbull22 divided the superficial radial nerve at the wrist and connected it directly to the ulnar nerve. Two years after surgery, he observed the return of pinprick sensation but not 2-point discrimination in the territory of the ulnar nerve. In lower-type injuries of the brachial plexus, sensation in the territory of the dorsal branch of the ulnar nerve is impaired.1 Hence, using the entire superficial radial nerve would produce complete anesthesia on the dorsal side of the hand. Alternatively,
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DISTAL SENSORY NERVE TRANSFERS
branches of the superficial radial nerve to the thumb could have been used, as proposed elsewhere for pure median nerve lesions.21,22 However, because of the possibility of causing neuropathic pain, which can be difficult to treat,23 we would hesitate to section superficial radial nerve branches at the wrist. Brown et al24 proposed coaptation of the dorsal branch of the ulnar nerve end-to-side to the median nerve at the wrist. Unfortunately, those authors did not provide results on sensory recovery. In our hands, end-to-side nerve repair yielded unsatisfactory results, both experimentally and clinically, such that we have abandoned this procedure.25,26 Our study has limitations, including the retrospective nature of our investigation and the limited number of patients. Also, the small number of patients did not permit us to stratify patients according to age or to the time interval between trauma and surgery. Nonetheless, we believe that in patients with lower-root brachial plexus injuries, these distal sensory nerve transfers may provide predictable restoration of protective sensation on the ulnar border of the hand and to the little finger, with limited risk. We advocate future prospective evaluation of these distal sensory nerve transfers, perhaps in a multi-institutional framework. REFERENCES 1. Bertelli JA, Ghizoni MF, Loureiro Chaves DP. Sensory disturbances and pain complaints after brachial plexus root injury: a prospective study involving 150 adult patients. Microsurgery 2011;31:93–97. 2. Bonnard C, Narakas A. Restoration of hand function after brachial plexus injury. Hand Clin 1995;11:647– 656. 3. Bertelli JA, Ghizoni MF. Brachialis muscle transfer to reconstruct finger flexion or wrist extension in brachial plexus palsy. J Hand Surg 2006;31A:190 –196. 4. Palazzi S, Palazzi JL, Caceres JP. Neurotization with the brachialis muscle motor nerve. Microsurgery 2006;26:330 –333. 5. Ozkan T, Ozer K, Gulgonen A. Restoration of sensibility in irreparable ulnar and median nerve lesions with use of sensory nerve transfer: long-term follow-up of 20 cases. J Hand Surg 2001;26A: 44 –51. 6. Tung TH, Mackinnon SE. Nerve transfers: indications, techniques, and outcomes. J Hand Surg 2010;35A:332–341. 7. Bertelli JA, Ghizoni MF. Very distal sensory nerve transfers in high median nerve lesions. J Hand Surg 2011;36A:387–393.
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8. Oberlin C, Teboul F, Severin S, Beaulieu JY. Transfer of the lateral cutaneous nerve of the forearm to the dorsal branch of the ulnar nerve, for providing sensation on the ulnar aspect of the hand. Plast Reconstr Surg 2003;112:1498 –1500. 9. Goubier JN, Teboul F. Management of hand palsies in isolated C7 to T1 or C8, T1 root avulsions. Tech Hand Up Extrem Surg 2008;12: 156 –160. 10. Doi K, Hattori Y, Kuwata N, Soo-heong T, Kawakami F, Otsuka K, et al. Free muscle transfer can restore hand function after injuries of the lower brachial plexus. J Bone Joint Surg 1998;80B:117–120. 11. Seddon H. Surgical disorders of the peripheral nerves. New York: Churchill Livingstone, 1975:303. 12. Bertelli JA. Neurocutaneous island flaps in upper limb coverage: experience with 44 clinical cases. J Hand Surg 1997;22A:515–526. 13. King PM. Sensory function assessment. A pilot comparison study of touch pressure threshold with texture and tactile discrimination. J Hand Ther 1997;10:24 –28. 14. van Brakel WH, Kets CM, van Leerdam ME, Khawas IB, Gurung KS. Functional sensibility of the hand in leprosy patients. Lepr Rev 1997;68:25–37. 15. Singh N, Armstrong DG, Lipsky BA. Preventing foot ulcers in patients with diabetes. JAMA 2005;12;293:217–228. 16. Letiévant JJE. Traité des sections nerveuses. Paris: J. B. Bailliére et Fils; 1873:41. 17. Jerosch-Herold C. Should sensory function after median nerve injury and repair be quantified using two-point discrimination as the critical measure? Scand J Plast Reconstr Surg Hand Surg 2000;34:339 –343. 18. Jerosch-Herold C. A study of the relative responsiveness of five sensibility tests for assessment of recovery after median nerve injury and repair. J Hand Surg 2003;28B:255–260. 19. Sperry RW. Functional results of crossing sensory nerves in the rat. J Comp Neurol 1943;78:59 –90. 20. Ruchelsman DE, Price AE, Valencia H, Ramos LE, Grossman JA. Sensory restoration by lateral antebrachial cutaneous to ulnar nerve transfer in children with global brachial plexus injuries. Hand 2010; 5:370 –373. 21. Brunelli GA. Sensory nerves transfers. J Hand Surg 2004;29B:557– 562. 22. Turnbull F. Restoration of digital sensation after transference of nerves. J Neurosurg 1963;20:238 –240. 23. Kandenwein JA, Richter HP, Antoniadis G. Is surgery likely to be successful as a treatment for traumatic lesions of the superficial radial nerve? Nervenarzt. 2006;77:175–176. 24. Brown JM, Yee A, Mackinnon SE. Distal median to ulnar nerve transfers to restore ulnar motor and sensory function within the hand: technical nuances. Neurosurgery 2009;65:966 –977. 25. Bertelli JA, dos Santos AR, Calixto JB. Is axonal sprouting able to traverse the conjunctival layers of the peripheral nerve? A behavioral, motor, and sensory study of end-to-side nerve anastomosis. J Reconstr Microsurg 1996;12:559 –563. 26. Bertelli JA, Ghizoni MF. Nerve repair by end-to-side coaptation or fascicular transfer: a clinical study. J Reconstr Microsurg 2003;19: 313–318.
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Distal Sensory Nerve Transfers in Lower-Type Injuries of the Brachial Plexus Jayme A. Bertelli, MD, PhD
Purpose To report the results of sensory nerve transfers to reconstruct sensation on the ulnar side of the hand in lower-type palsies of the brachial plexus. Methods From 2007 to 2009, we operated on 6 men and 2 women with a lower-type injury of the brachial plexus and observed them for a minimum of 24 months. The mean interval between the injury and surgery was 8 months (SD ⫾ 8.6 mo). Before surgery, we documented anesthesia on the ulnar side of the hand in all patients. Donor nerves included cutaneous branches of the median nerve to the palm (n ⫽ 5) or the palmar cutaneous branch of the median nerve (n ⫽ 3). The ulnar proper digital nerve of the little finger was the recipient nerve. We evaluated sensory recovery by assessing static 2-point discrimination and sensation to Semmes-Weinstein monofilaments. Results According to the British Medical Council system of evaluation, 5 patients scored S3 and 3 scored S3⫹. Conclusions In lower-type injuries of the brachial plexus, transfer of median nerve branches that innervate the palm of the hand to the ulnar proper digital nerve of the little finger predictably restored protective sensation on the ulnar side of the hand. (J Hand Surg 2012;37A:1194–1199. Copyright © 2012 by the American Society for Surgery of the Hand. All rights reserved.) Type of study/level of evidence Therapeutic IV. Key words Brachial plexus, lower root palsy of the brachial plexus, nerve transfer, sensory reconstruction. brachial plexus injuries can be roughly classified into upper- and lower-type injuries. With uppertype injuries, the C5 and possibly C6 and C7 roots are affected, and despite clinical motor paralysis, hand sensation is largely preserved and no sensory reconstruction is needed.1 Conversely, with lower-type injuries, the T1 and, possibly, C8 and C7 roots are involved. The ulnar border of the hand is insensate and would likely
A
CCORDING
TO
ROOT
INVOLVEMENT,
From the Center of Biological and Health Sciences, Department of Neurosurgery, University of the South of Santa Catarina (Unisul), Tubarão; and the Department of Orthopedic Surgery, Governador Celso Ramos Hospital, Florianópolis, Santa Catarina, Brazil. Received for publication November 29, 2011; accepted in revised form February 27, 2012. No benefits in any form have been received or will be received related directly or indirectly to the subject of this article. Corresponding author: Jayme A. Bertelli, MD, PhD, Rua Newton Ramos 70, Apto 901, Florianópolis-SC, 88015395, Brazil; e-mail: [email protected]. 0363-5023/12/37A06-0014$36.00/0 http://dx.doi.org/10.1016/j.jhsa.2012.02.047
1194 䉬 © ASSH 䉬 Published by Elsevier, Inc. All rights reserved.
benefit from sensory reconstruction.1 Loss of sensation on the ulnar side of the hand predisposes to injury, because the ulnar side usually is used to support the hand while the radial fingers carry out manipulation. Sensation on the ulnar border of the hand is particularly important if the hand is ever placed on a potentially damaging surface, such as a hot stove. Also, because of the absence of sensation on the tip of the little finger, minor repetitive trauma may be neglected, resulting in skin breakdown and infections. In lower-type palsies, the roots are always avulsed, and reconstructive surgery for hand motion relies on nerve and tendon transfers.2– 4 Nerve transfers for motor reconstruction of median and ulnar nerve lesions have been reported.5–7 However, specifically for sensory reconstruction in lower-type lesions of the brachial plexus, we identified 3 reports. Oberlin et al8 and Goubier and Teboul9 transferred the lateral antebrachial cutaneous nerve with the help of a long graft to the
DISTAL SENSORY NERVE TRANSFERS
dorsal branch of the ulnar nerve. Doi et al10 transferred intercostal nerves to the ulnar nerve. We report the results of direct nerve transfers for sensory reconstruction along the ulnar border of the hand in lower-type injuries of the brachial plexus. Donor nerves included cutaneous branches of the median nerve to the palm or the palmar cutaneous branch of the median nerve. The ulnar proper digital nerve of the little finger was the recipient nerve. MATERIALS AND METHODS In advance of any data collection, the local ethics committee approved the protocol of the study. Patients provided written informed consent before participation, in accordance with the Declaration of Helsinki guiding biomedical research involving human subjects. From 2007 to 2009, we operated on 6 men and 2 women with lower-type injuries of the brachial plexus and observed them for a minimum of 24 months (Table 1). Their average age was 34 years (SD ⫾15 y), and the mean interval between the initial injury and surgery was 8 months (SD ⫾ 8.6 mo). All had lower root avulsion documented by computed tomographic myelography (n ⫽ 4) or magnetic resonance imaging (n ⫽ 4). All presented with a Horner sign, except for 1 patient with a prosthetic eye replacement resulting from a previous injury. In each patient, we demonstrated anesthesia on the ulnar side of the hand by the absence of perception of a 33.1-g/mm2 monofilament, and of pain when the skin was pinched with flat forceps. We reconstructed sensation along the ulnar border of the hand using distal nerve transfers. If perception of 19.3-g/mm2 Semmes-Weinstein monofilaments (protective sensation) was preserved in the center of the palm, we used as donors cutaneous branches of the median nerve to the skin (Fig. 1) just distal to the carpal tunnel. We used these median nerve cutaneous branches either isolated (n ⫽ 3) or combined (n ⫽ 2) with fascicles of the ulnar proper digital nerve of the index finger (Fig. 2) if the caliber of the cutaneous branches failed to cover the entire surface of the distal stump of the ulnar proper digital nerve of the little finger. Before harvesting fascicles of the proper digital nerve of the index finger, we determined that pulp sensation was normal on monofilament testing (ie, preserved perception of a 1.5-g/mm2 monofilament). In the case of absent protective sensation over the zone just distal to the carpal tunnel, we used the palmar cutaneous branch of the median nerve for transfer, provided that perception of a 19.3-g/mm2 monofilament was preserved over the thenar region (n ⫽ 3). After proximal dissection, the ulnar proper digital nerve
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of the little finger was the recipient nerve in these 3 patients (Fig. 3). At final evaluation, we tested for static 2-point discrimination on the tip of the small finger using a DiskCriminator testing device (Connecticut Bioinstruments, Baltimore, MD). On the ulnar border of the little finger and hand, we investigated sensory thresholds using Semmes-Weinstein monofilaments in accordance with methods reported elsewhere.7 We used 4 sets of monofilaments. According to the manufacturer (Sorri, Bauru, Sao Paulo, Brazil), the 0.05, 0.2, 2.0, and 4.0 monofilaments produce pressures of 1.5, 11.1, 19.3, and 33.1 g/mm2, respectively. To map the reinnervated cutaneous territory, we considered referred sensation corresponding to the donor nerve primary zone of innervation as a guideline. We grasped the skin on the ulnar side of the hand with a flat forceps with increasing firmness until pain was perceived either in the central part of the palm or in the thenar region. This denoted that reinnervation stemmed from our nerve transfer rather than from spontaneous regeneration of adjacent nerves. We repeated this all over the ulnar border of the hand. Then, with a skin marker, we delineated the cutaneous territory presenting referred sensation, for photographing. We also determined results according to British Medical Research Council standards.11 We rated the patient’s score S3 when that patient perceived contact from a 33.1-g/mm2 monofilament, and S3⫹ when he perceived 2 points less than 10 mm apart. For detection of donor site deficits after nerve harvesting, we applied monofilament testing on the tip of the index finger, the thenar region, and the central part of the palm. For the thenar region and palm, we only applied 19.3-g/mm2 monofilaments. An examiner blinded to which nerve had been transferred conducted final sensory assessments. RESULTS All patients improved from baseline (Table 1), including those with longstanding lesions. The territory of sensory recovery extended to the tip of the little finger and the ulnar border of the hand. We observed recovery of 2-point discrimination in 3 of the 8 patients. In 2 of these 3 patients, we had connected branches of the median nerve to the palm together with fascicles of the ulnar proper digital nerve of the index to the ulnar proper digital nerve of the little finger. In the remaining case, we only used branches of the median nerve to the palm. Preoperatively or shortly after surgery, 4 of the 8 patients experienced a burn in the hypothenar region (n ⫽ 1) or on the little finger (n ⫽ 3).
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TABLE 1.
Patient Data Summary
Age/Sex
1
20, M
3
Palmar branch of median nerve to ulnar proper digital nerve of little finger
24
2
18, M
28
Cutaneous branches to palm plus fascicles of ulnar proper digital nerve of index to ulnar proper digital nerve of little finger
48
3
48, M
12
Cutaneous branches to palm to ulnar proper digital nerve of little finger
24
4
20, M
4
Cutaneous branches to palm plus fascicles of ulnar proper digital nerve of index to ulnar proper digital nerve of little finger
24
5
30, M
4
Palmar branch of median nerve to ulnar proper digital nerve of little finger
36
6
55, F
4
Palmar branch of median nerve to ulnar proper digital nerve of little finger
36
7
28, F
6
Cutaneous branches of palm to ulnar proper digital nerve of little finger
24
8
50, M
3
Cutaneous branches to palm to ulnar proper digital nerve of little finger
27
Surgery
BMRC, British Medical Research Council; ⫹, pain perception recovery.
Evaluation After Surgery (mo)
2-Point Discrimination (mm)
7
8
7
Monofilaments (Manufacturer’s Calculated Pressure [g/mm2])
Pain Perception
Territory of Reinnervation
BMRC
⫹
Distal ulnar border of hand plus little finger
S3
19.3
⫹
Distal ulnar border of hand plus little finger
S3⫹
11.1
⫹
Distal ulnar border of hand plus little finger
S3
19.3
⫹
Distal ulnar border of hand plus little finger
S3⫹
⫹
Distal ulnar border of hand plus little finger
S3
33.1
⫹
Distal ulnar border of hand plus little finger
S3
19.3
⫹
Distal ulnar border of hand plus little finger
S3⫹
19.3
⫹
Distal ulnar border of hand plus little finger
S3
DISTAL SENSORY NERVE TRANSFERS
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Interval Between Accident and Surgery (mo)
DISTAL SENSORY NERVE TRANSFERS
FIGURE 1: Intraoperative photograph of the palmar region of a left hand demonstrating transfer of a cutaneous branch of the median nerve (CB) to the ulnar proper digital nerve of the little finger (PL). P, ulnar proper digital nerve of the index finger. In the inset, we show the nerves after microsurgical coaptation.
FIGURE 2: Intraoperative view of the palmar region of a left hand, showing transfer (black arrow) of a cutaneous branch to the palm together with 2 fascicles of the ulnar proper digital nerve to the index to the ulnar proper digital nerve of the little finger. In the inset, we show the skin incisions used for the surgical procedure. P, ulnar proper digital nerve of the index finger.
Afterward, no other injuries on the ulnar side of the hand occurred. During our assessment for nociceptive recovery, we demonstrated referred sensation in all patients. However, none reported referred sensation adversely affecting daily activities. There were no donor site deficits on the index finger or loss of protective sensation in the palm or thenar region. Pain reports were absent.
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FIGURE 3: Intraoperative view of the left wrist showing transfer of the palmar cutaneous branch of the median nerve (PM) to the ulnar proper digital nerve of the little finger (PL). We used the incision at the distal palmar crease to correct metacarpophalangeal hyperextension. We also located the ulnar proper digital nerve of the little finger through this incision. We elongated the wrist incision to transfer the brachialis via a tendon graft to the flexor pollicis longus and flexor digitorum profundus tendons.
DISCUSSION In our series of 8 patients, transfer of either the palmar branch or cutaneous branches to the palm of the median nerve restored at least S3 sensation on the ulnar side of the hand. We based our indications to use one or the other nerve on preoperative screening for preserved sensation on the palm. Our first choice as donor nerves was the cutaneous branches of the median nerve in the palm because nerve coaptation is closer to cutaneous targets on the ulnar side of the little finger compared with nerve coaptation at the wrist, in which case the palmar cutaneous branch of the median nerve was the donor nerve. Lesions affecting the 3 lower roots of the brachial plexus tended to exhibit more extended sensory loss.1 However, even in such extended lesions, sensation over the thenar region was preserved, allowing for the use of the palmar cutaneous branch of the median nerve as the donor. In 3 patients, transfer of cutaneous branches of the median nerve, either combined with or separate from fascicles of the ulnar proper digital nerve to the index finger, restored 2-point discrimination on the tip of the little finger. The territory of cutaneous reinnervation included the ulnar border of the little finger and distal palm. After harvesting median nerve branches to the palm for transfer, we observed no donor site deficits or pain reports. Possibly, superimposed innervation exists between the palmar cutaneous branch of the median nerve
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and the lateral antebrachial cutaneous nerve, and between the palmar cutaneous branch of the median nerve and branches to the palm. When we harvested fascicles of the proper digital nerves to the index finger, normal sensation at the fingertip persisted. This is in agreement with our previous report in which we used fascicles of the proper digital nerves to the index finger to reinnervate skin flaps.12 According to the British Medical Research Council scale, S3 is related to return of superficial cutaneous pain and tactile sensibility.11 Because no objective parameter has been defined to represent superficial cutaneous pain and tactile sensibility, we used as a guideline the perception of 19.3-g/mm2 monofilament, which is related to protective sensation in the hand.13 Hence, in our analysis, a result scoring S3 meant that the patient recovered protective sensation at least. However, we believe that perception of 19.3 g/mm2 is not just the perception of a harmful stimulus. In fact, perception of 19.3 g/mm2 correlates positively with texture discrimination.14 In the diabetic foot, ulcers are associated with lack of perception of 10-g/mm2 monofilaments.15 However, testing sensation with heavier monofilaments may produce finger motion or reverberation of the stimuli on proximal zones. More than a century ago, Letiévant16 demonstrated that patients could perceive touching on totally necrotic skin on the fingertip due to mechanical stimulus perception in healthy proximal zones. Here, we believe that testing painful sensation with forceps would be preferable—in particular, if the amount of pressure on the forceps tip could be measured using a gauge. The next higher British Medical Research Council grade is S3⫹, which denotes some recovery of 2-point discrimination.11 However, 2-point discrimination may not effectively correlate to sensibility recovery.17 Jerosch-Herold18 observed that as much as 71% of 41 patients with repair of the median nerve at the wrist recovered no measurable 2-point discrimination 18 months after repair. This author considered that the 2-point discrimination test was not reliable to document recovery, which was more accurately documented by monofilaments screening. To determine the territory of cutaneous reinnervation, we tested nociceptive perception using forceps and referred sensation to the autonomous zone of the donor nerve. Faulty location is a common finding after sensory nerve transfer, in particular when different or distant zones are involved, as in our cases in which we crossed median and ulnar nerve branches.7 This does not mean that faulty location eliminates the benefits of nerve crossing. Patients can learn to cope with faulty location. In the set of sensory nerve crossing, Sperry19
believed that voluntary control, which depends on higher brain centers, can be learned: for instance, the removal of a painful stimulus applied to a reinnervated zone. This would result from learning experiences of fruitful or fruitless reactions. On the other hand, Sperry19 considered spinal reflexes not to be modifiable. In a series of 13 patients with lower-type injuries of the brachial plexus, Gobier and Teboul9 observed S2 recovery after transfer of the lateral antebrachial cutaneous nerve to the dorsal branch of the ulnar nerve with an intercalated 15-cm-long sural nerve graft. In 3 children aged 5.0, 6.5, and 7.0 years, with global obstetric brachial plexus injury, Ruchelsman et al20 divided the lateral antebrachial cutaneous nerve and implanted the proximal stump termino-laterally into the ulnar nerve. All 3 children recovered innervation on the ulnar border of the hand, as demonstrated by skin wrinkling after immersing the hands in warm water. Doi et al10 reported their results with intercostal nerve transfer to the ulnar nerve in 3 patients with lower-type brachial plexus injuries. Two of the patients recovered superficial pain and touch sensation, whereas the third patient did not. In 2 patients with brachial plexus injury who had partially recovered sensation in the middle finger (S3⫹), Brunelli21 transferred a proper digital nerve of the middle finger to the ulnar proper digital nerve of the little finger. In 1 of his patients, the end result was S2⫹; in the other it was S1. With our technique, we employed no nerve grafts and we performed nerve coaptation close to end organs. Likely, these 2 advantages contributed to our improved sensory recovery even many months after injury. Because of anesthesia along the ulnar border of the hand, the cases presented here theoretically could have been treated as high ulnar nerve lesions, but in our patients, the roots to the median nerve were also injured. Because we were concerned about donor site deficits, we elected not to harvest donor nerves of important zones, such as the entire ulnar proper digital nerve of the index finger, as proposed by Ozkan et al5 for pure ulnar nerve lesions. In a 13-year-old patient with ulnar and median nerve lesions in the arm, Turnbull22 divided the superficial radial nerve at the wrist and connected it directly to the ulnar nerve. Two years after surgery, he observed the return of pinprick sensation but not 2-point discrimination in the territory of the ulnar nerve. In lower-type injuries of the brachial plexus, sensation in the territory of the dorsal branch of the ulnar nerve is impaired.1 Hence, using the entire superficial radial nerve would produce complete anesthesia on the dorsal side of the hand. Alternatively,
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branches of the superficial radial nerve to the thumb could have been used, as proposed elsewhere for pure median nerve lesions.21,22 However, because of the possibility of causing neuropathic pain, which can be difficult to treat,23 we would hesitate to section superficial radial nerve branches at the wrist. Brown et al24 proposed coaptation of the dorsal branch of the ulnar nerve end-to-side to the median nerve at the wrist. Unfortunately, those authors did not provide results on sensory recovery. In our hands, end-to-side nerve repair yielded unsatisfactory results, both experimentally and clinically, such that we have abandoned this procedure.25,26 Our study has limitations, including the retrospective nature of our investigation and the limited number of patients. Also, the small number of patients did not permit us to stratify patients according to age or to the time interval between trauma and surgery. Nonetheless, we believe that in patients with lower-root brachial plexus injuries, these distal sensory nerve transfers may provide predictable restoration of protective sensation on the ulnar border of the hand and to the little finger, with limited risk. We advocate future prospective evaluation of these distal sensory nerve transfers, perhaps in a multi-institutional framework. REFERENCES 1. Bertelli JA, Ghizoni MF, Loureiro Chaves DP. Sensory disturbances and pain complaints after brachial plexus root injury: a prospective study involving 150 adult patients. Microsurgery 2011;31:93–97. 2. Bonnard C, Narakas A. Restoration of hand function after brachial plexus injury. Hand Clin 1995;11:647– 656. 3. Bertelli JA, Ghizoni MF. Brachialis muscle transfer to reconstruct finger flexion or wrist extension in brachial plexus palsy. J Hand Surg 2006;31A:190 –196. 4. Palazzi S, Palazzi JL, Caceres JP. Neurotization with the brachialis muscle motor nerve. Microsurgery 2006;26:330 –333. 5. Ozkan T, Ozer K, Gulgonen A. Restoration of sensibility in irreparable ulnar and median nerve lesions with use of sensory nerve transfer: long-term follow-up of 20 cases. J Hand Surg 2001;26A: 44 –51. 6. Tung TH, Mackinnon SE. Nerve transfers: indications, techniques, and outcomes. J Hand Surg 2010;35A:332–341. 7. Bertelli JA, Ghizoni MF. Very distal sensory nerve transfers in high median nerve lesions. J Hand Surg 2011;36A:387–393.
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8. Oberlin C, Teboul F, Severin S, Beaulieu JY. Transfer of the lateral cutaneous nerve of the forearm to the dorsal branch of the ulnar nerve, for providing sensation on the ulnar aspect of the hand. Plast Reconstr Surg 2003;112:1498 –1500. 9. Goubier JN, Teboul F. Management of hand palsies in isolated C7 to T1 or C8, T1 root avulsions. Tech Hand Up Extrem Surg 2008;12: 156 –160. 10. Doi K, Hattori Y, Kuwata N, Soo-heong T, Kawakami F, Otsuka K, et al. Free muscle transfer can restore hand function after injuries of the lower brachial plexus. J Bone Joint Surg 1998;80B:117–120. 11. Seddon H. Surgical disorders of the peripheral nerves. New York: Churchill Livingstone, 1975:303. 12. Bertelli JA. Neurocutaneous island flaps in upper limb coverage: experience with 44 clinical cases. J Hand Surg 1997;22A:515–526. 13. King PM. Sensory function assessment. A pilot comparison study of touch pressure threshold with texture and tactile discrimination. J Hand Ther 1997;10:24 –28. 14. van Brakel WH, Kets CM, van Leerdam ME, Khawas IB, Gurung KS. Functional sensibility of the hand in leprosy patients. Lepr Rev 1997;68:25–37. 15. Singh N, Armstrong DG, Lipsky BA. Preventing foot ulcers in patients with diabetes. JAMA 2005;12;293:217–228. 16. Letiévant JJE. Traité des sections nerveuses. Paris: J. B. Bailliére et Fils; 1873:41. 17. Jerosch-Herold C. Should sensory function after median nerve injury and repair be quantified using two-point discrimination as the critical measure? Scand J Plast Reconstr Surg Hand Surg 2000;34:339 –343. 18. Jerosch-Herold C. A study of the relative responsiveness of five sensibility tests for assessment of recovery after median nerve injury and repair. J Hand Surg 2003;28B:255–260. 19. Sperry RW. Functional results of crossing sensory nerves in the rat. J Comp Neurol 1943;78:59 –90. 20. Ruchelsman DE, Price AE, Valencia H, Ramos LE, Grossman JA. Sensory restoration by lateral antebrachial cutaneous to ulnar nerve transfer in children with global brachial plexus injuries. Hand 2010; 5:370 –373. 21. Brunelli GA. Sensory nerves transfers. J Hand Surg 2004;29B:557– 562. 22. Turnbull F. Restoration of digital sensation after transference of nerves. J Neurosurg 1963;20:238 –240. 23. Kandenwein JA, Richter HP, Antoniadis G. Is surgery likely to be successful as a treatment for traumatic lesions of the superficial radial nerve? Nervenarzt. 2006;77:175–176. 24. Brown JM, Yee A, Mackinnon SE. Distal median to ulnar nerve transfers to restore ulnar motor and sensory function within the hand: technical nuances. Neurosurgery 2009;65:966 –977. 25. Bertelli JA, dos Santos AR, Calixto JB. Is axonal sprouting able to traverse the conjunctival layers of the peripheral nerve? A behavioral, motor, and sensory study of end-to-side nerve anastomosis. J Reconstr Microsurg 1996;12:559 –563. 26. Bertelli JA, Ghizoni MF. Nerve repair by end-to-side coaptation or fascicular transfer: a clinical study. J Reconstr Microsurg 2003;19: 313–318.
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